PLASTIDS IN THE ROOTS OF PHASEOLUS VULGARIS
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1 New Phytol. (1983) 94, PLASTIDS IN THE ROOTS OF PHASEOLUS VULGARIS BY J. M. WHATLEY Botany School, South Parks Road, Oxford OXl 3RA {Accepted 10 February 1983) SUMMARY In roots of Phaseolus vulgaris plastid development takes place from the apical meristem both upwards into the root proper and downwards into the root cap. The maximum state of plastid development seems to be achieved in the cortical cells of that part of the primary root associated with mature root hairs. However in these cortical cell plastids the thylakoid system is very limited in extent and no true prolamellar bodies are formed. Farther from the apex of the root proper, in the zone of mature lateral roots, the plastids appear to have undergone dedifferentiation and to have lost whatever thylakoids they once contained.both the rate of plastid development and the patterns of production of ancillary plastid structures, including starch and membrane-bound bodies, vary in different cellfiles. The differential distribution of these and other plastid features are summarized in the accompanying diagrams. INTRODUCTION Little is known about the ultrastructure or the function of plastids in roots. Most ultrastructural investigations have been confined to the root tip (Newcomb, 1967) or have been concerned either with the starch-containing statoliths in root caps and their role in geoperception (GrifiSths and Audus, 1964; Juniper and French, 1970; Barlow and Grundwag, 1974), or with the conversion of root proplastids into chloroplasts during greening (Heltne and Bonnett, 1970; Salema, 1971; Oliveira, 1982) a process which has been shown in excised roots, to have different light requirements from those in leaves (summarized in Bjorn, 1980). It has long been known that in most roots cellular differentiation follows a bidirectional course, the first sequence extending from the apical meristem upwards through the root p-roper and the second downwards through the root cap (Esau, 1965). The progress of cellular differentiation in roots can be identified by following individual cell files which display successive stages of development as a spatial sequence. The small green root of the water fern, Azolla pinnata, develops from a single apical cell by means of a limited number of precise divisions and these have recently been described in some detail by Gunning and his associates (Gunning, 1978; Gunning, Hughes and Hardham, 1978). It is therefore comparatively easy in roots of this species to determine the exact developmental age and relative stage of differentiation of each individual cell within the root proper.whatley and Gunning (1981) found that, in the root proper of A. pinnata, chloroplast development, like cell development, followed a spatial sequence extending upwards from the apical cell. The state of chloroplast development was judged on the basis of plastid size and the extent of the thylakoid system; the number of plastid profiles within each cell section was also assessed. The maturing chloroplasts within each cell file were distinctive in their rates of development and in the sizes and numbers finally X/83/07038H-11 S03.00/ The New Phytologist
2 382 J. M. WHATLEY achieved. The spatial sequence of plastid development observed in individual roots of Azolla could also be followed as a temporal sequence in roots of increasing age. Spatial sequences of plastid development have also been identified in roots of Convolvulus arvensis during greening (Heltne and Bonnett, 1970) and in the sieve elements in roots of several species (Esau and Gill, 1973) as well as in temporal sequence during root cap regeneration in Zea mays (Barlow and Grundwag, 1974). However, few details are available about how plastids in non-green roots (i.e. most roots) vary in structure during development or in cells at different sites within individual roots. The purpose of this study has been to map the distribution of a number of plastid features within a young non-green root and to assess the developmental pathways which gave rise to these patterns of distribution. The criteria used to assess the state of plastid development in the non-green roots of Phaseolus vulgaris are the five sequential basic stages of plastid development which it has been suggested elsewhere are common to plastid differentiation in all organs (Whatley, 1977, 1978): Stage 1, the more or less spherical eoplast, with stroma but little thylakoid membrane; stage 2, the amyloplast, in which starch begins to accumulate; stage 3, the amoeboid or pleomorphic plastic, from which much of the starch has often been lost; stage 4, the pre-granal plastid, usually discoid in shape with an extending system of single, perforated thylakoids and incipient grana or bithylakoids; stage 5, the mature chloroplast, with continuous thylakoids and true grana. This basic pathway has been identified as a temporal sequence in several organs of P. vulgaris grown in the light or in the darkness, as both a temporal sequence and as a spatial sequence extending upwards from the basal meristem in leaves of the grass Z. mays (Whatley, 1977, 1978, unpublished results) and as a spatial sequence in the leaves oi Hordeum vulgare (Wellburn, Robinson and Wellburn, 1982). When different environmental conditions are experienced either externally (e.g. absence of light) or internally (e.g. in different organs or in different types of cell) plastid development may be diverted from its normal course and thylakoid extension may be temporarily or permanently blocked. Ancillary structures such as the proiamellar bodies of dark-grown leaves may then be formed, probably as a result of the production of some precursor materials in excess of requirements (Whatley, 1977). Evidence relating to the universality of this single, basic morphogenetic pathway of plastid development and the various light- or dark-induced disturbances which may affect it has recently been reviewed by Klein (1982). MATERIALS AND METHODS Seeds of P. vulgaris, cv. Canadian Wonder were soaked for 5 h in distilled water, stripped of their seed coats, planted in soil and kept in a growth cabinet at 24 C under a regime of 12 h light and 12 h dark. After 5 days, the tips of ten and upper segments of five primary roots were detached and prepared for examination under the electron microscope. From these roots the basal 2-5 to 3 mm, including the cap, and segments of cortex 1 mm in length from the zones of mature root hairs and lateral roots were removed. The tissue was fixed in 3% glutaraldehyde in cacodylate buffer, ph 7 2, post-fixed in 1 % osmium tetroxide, dehydrated in a graded ethanol series, transferred to acetone and embedded in Epon 812. The embedded root segments were examined in either longitudinal section (most samples) or in transverse section. Data shown in the tip portion of the distribution diagrams presented in the Results section were compiled from information
3 Plastids in roots 383 obtained from consecutive sequences of transverse sections cut at intervals of 0*2 mm upwards from the cap. Data obtained from median longitudinal sections of other root tips were in agreement with that from the root selected for illustration. RESULTS In the roots of P. vulgaris there can be distinguished two spatial sequences of plastid development which parallel those of cell differentiation [Figs 1; 2(a) to (h); 3(a), (b)]. The first sequence (stages 1 to 4) extends upwards through the root from Laterol root _ zone Root hoir zone I5r 10 Root tip_ (2-5 mm) Section level I Fig. 1. The sequence of plastid development in a root of P. vulgaris. 1, Eoplast; 1', dediflerentiated plastid = eoplast; 2, amyloplast; 3, amoeboid plastid; 4, pre-granal plastid; -, direction of plastid differentiation; -, direction of plastid dedifferentiation;, level of earliest sieve element plastids. a core of cells at the extreme tip of the root proper; the second sequence (stages 1 to 3) extends downwards and outwards through the root cap. The same basic sequence of developmental stages was found in all the roots examined, but there was some variation between roots in the levels at which particular plastid stages were attained. Plastids at the same stage of development in different roots also showed quantitative differences, e.g. in the sizes of their membrane-bound bodies or in the numbers and sizes of their starch grains. In each root proper, the same sequence of development could be identified in all cellfiles,though within different files, transformation of plastids from one stage of development to the next was found at different distances from the apex. Preliminary observations on older and younger roots of Phaseolus suggest that, as in the Azolla roots, the older the root, the closer to the meristem is a particular stage of development first attained, i.e. there is acropetal drift. In roots of Phaseolus the stage 1 eoplasts [Fig. 2(a)l and, initially, also, the stage 2 amyloplasts [Fig. 2(b), (e)] may be either rod-shaped or spherical and the 13 ANP 94
4 J. M. WHATLEY 384 i. \ -1 ' I. < : : r.' Fig. 2 -
5 Plastids in roots 385 succeeding stage 3 amoeboid or pleomorphic phase [Fig. 2(c), (f), (g)] seems to be much less transitory than it is in leaves. Serial sectioning shows that the amoeboid plastids in the cortical cells of the root proper are generally of much greater length than those in the root cap or in leaves and are often ' branched' and highly convoluted. These root plastids usually contain starch which tends to be concentrated in distended pockets (frequently at the ends of branches) and these pockets are linked by narrower strands containing only stroma. Towards the upper part of the root tip segment the plastids are no longer markedly pleomorphic [Fig. 2(h)]. Within the root cap, the maximum development achieved by plastids is stage 3 [Fig. 2(c)]; the cells in which these plastids are found have reached the periphery of the cap and are being sloughed off. Within the root proper the maximum state of plastid development seems to be found in the cortex of the root hair zone where it approaches that of stage 4 [Fig. 3(a)]. The discoid plastids of the root hair zone have an apparently extending system of single, perforated thylakoids with incipient grana which, however, lacks both the extent and the characteristic more or less spiral, spatial organization of stage 4 plastids of both green and non-green leaves [Fig. 3(d), (e)]. Farther from the root tip, in the cortex of the lateral root zone, the plastids are spherical in shape and are unusual in that they seem to be quite devoid of thylakoids [Fig. 3(b)]. Though I have examined many sections (including serial sections) I have not observed a single plastid profile within this zone in which there is even the smallest fragment of thylakoid membrane. However, cells in this zone are highly vacuolated and each thin section contains few plastid profiles, so further investigation is required before a complete absence of thylakoid material can be confirmed. Other plastid components In the roots, as in the leaves, there are superimposed upon the basic stages of plastid development variations associated with the accumulation of other plastid components, viz. phytoferritin, starch, thylakoid or tubular complexes and membrane-bound bodies. The pattern of distribution within the root differs for each of these components (Figs 4 and 5), and this diversity emphasizes the individuality of plastid populations in different types of cell. In the small Azolla roots previously examined it was possible to analyse variations along individual cell files. Analysis of the larger Phaseolus roots was less detailed but plastids in cells of the inner and outer cortex, for example, clearly differ in their relative rates and patterns of development, though the overall sequence is the same in cells of the two regions. Phytoferritin (Fig. 5) seems to be present in more or less equal amounts in plastids of all cells, from the root cap to the lateral root zone. Because other components are absent from the stroma of plastids in the cortex of the lateral root Fig. 2. (a) An eoplast (perhaps dividing) from the root apex, x (b) An amyloplast from the centre of the root cap. X (c) An amoehoid plastid with typical electron-dense stroma from the periphery of the root cap. x (d) A maturing sieve element plastid. x (e) A developing amyloplast from the inner cortex (Section level 6 in Fig. 1). x (f) A 'branched' amoeboid plastid from the outer cortex (Section level 11. x (g) All the plastid profiles (arrows) in this group belong to the same amoeboid plastid. x (h) A plastid from the outer cortex (Section level 15); it is not markedly amoeboid and it contains less starch than plastids at immediately lower section levels, x mg. Membrane-bound body with granular contents; p, phytoferritin; t, thylakoid complex. 13-2
6 386 J. M. WHATLEY N vr \ Cb>.. - -; /' \ V..-- "' * '; 'A cn-^' i,. : -..! ; ' : Fig ' : ;
7 Plastids in roots 387 (Fig. 4) (Fig. 5) Fig. 4. A representation of the distribution of starch and membrane-bound bodies in a Phaseolus root.y., Starch;!, membrane-bound bodies. Fig. 5. A representation of the distribution of phytoferritin and thylakoid complexes in a Phaseolus root.:;., Phytoferritin;, thylakoid complexes. zone [Fig. 3(b), the phytoferritin here is particularly conspicuous and it may well occupy a larger proportion of the total stromal volume than in plastids in other parts of the root. The initiation of starch accumulation marks the onset of the second stage of plastid development. However the extent to which starch is accumulated during stage 2, or is retained or lost during later stages, varies in different types of cell. Figure 6 shows the differing quantities of starch present in plastids of the inner and outer cortex, the stele parenchyma and the root cap at different distances from the cap junction. The accumulation and loss of starch in cells of the outer cortex at levels closer to the apex than in cells of the inner cortex (Fig. 4) may well reflect the greater developmental age of the cells of the outer cortex (Esau, 1965). Starch is scarce in cortical cell plastids of the root hair zone and absent from plastids in the lateral root zone. The pattern of starch distribution within the root is shown Fig. 3. (a) A pre-granal plastid with a poorly developed system of perforated thylakoids and incipient grana (arrows), from the cortex of the root hair zone. Unusually this plastid contains some starch, x (b) An eoplast from the cortex of the lateral root zone, x (c) A thylakoid complex in a plastid from the apex of the root proper, x (d) thylakoid complex in a leaf plastid from a 5-day Phaseolus seedling grown in the light, x (e) A true prolamellar body in a leaf etioplast from a 5-day Phaseolus seedling grown in the dark, x (f) A thylakoid complex in a hypocotyl plastid from a 5-day Phaseolus seedling grown in the dark, x (g) Membrane-bound bodies with crystalline contents linked to a thylakoid complex in a plastid from the outer cortex, x (h) A membrane-bound body with granular contents in a root cap plastid. X me. Membrane bound body with crystalline contents; mg, membrane-bound body with granular contents; p, phytoferritin; plb, prolammellar body; t, thylakoid complex.
8 388 J. M. WHATLEY Section number Root cap Section number Root proper Fig. 6. The numbers of starch grains and the areas occupied by starch grains in plastids in different parts of the root proper, o, number of starch grains per plastid profile in the outer cortex;, number of starch grains per plastid profile in the inner cortex;, number of starch grains per plastid profile in the stelar parenchyma;, number of starch grains per plastid profile in the root cap; O. area occupied by starch grains per plastid profile in the outer cortex; #, area occupied by starch grains per plastid profile in the inner cortex; Q. area occupied by starch grains per plastid profile in the root cap. hoir in Figure 4 which also emphasizes the marked accumulation of starch in plastids in the central cells of the root cap. Small thylakoid or tubular complexes [Fig. 3(c), (g)], which somewhat resemble a true proiamellar body but lack its paracrystalline organization [Fig. 3(e)], are present in some plastids of the root cap and in many plastids at the apex of the root paper. The frequency with which these complexes are found appears to decline from the apex upwards through the root. Few complexes have been observed in plastids of the root hair zone and none in plastids of the lateral root zone (Fig. 5). Membrane-bound bodies containing crystalline [Fig. 3(g)] or, more commonly, granular [Fig. 3(h) material, which may be proteinaceous, are present in plastids of cells towards the periphery of the root cap and, within the root tip proper, in plastids entering or at stage 3. These bodies, like the thylakoid complexes, appear to decline in frequency upwards through the root tip segment: membrane-bound bodies are not found in plastids of either the root hair or the lateral root zone (Fig. 4). In the root proper, the membrane-bound bodies appear to be acquired only a short distance from the apex by plastids in the epidermis and outer cortex but further from the apex by plastids of the inner cortex. In the upper part of the root tip these bodies are retained only by epidermal plastids and by plastids of the inner cortex. By contrast, thylakoid complexes are present in plastids of cells throughout the apex of the root proper and in some plastids of the inner cortex even in the root hair zone but are absent from epidermal cell plastids close to the apex. No membrane-bound bodies and few thylakoid complexes have been observed in plastids of any type of cell within the stele. In general, plastid differentiation within the stele takes place farther from the tip, and plastids are conspicuously smaller than in cortical cells. However, maturing sieve element plastids [Figs 1; 2(d)], indistinguishable from their counterparts in Phaseolus leaves, can first be identified in cells quite close to the apex of the root proper and adjacent to other
9 Plastids in roots 389 cells of the stele in which plastids have not yet differentiated beyond stage 1. This observation is in agreement with that of Esau (e.g. Esau and Gill, 1973) and others that development of these distinctive plastids is the first visible sign of differentiation of the cells which will later become sieve elements. DISCUSSION In the non-green roots of P. vulgaris., the five successive basic stages of plastid development can be traced as a spatial sequence of differentiation extending along individual cell files from the apical meristem upwards into the root proper and downwards into the root cap. These two sequences parallel the bidirectional course of cellular differentiation characteristic of most roots. The transformation of both plastids and cells from one stage of development to the next takes place at different distances from the apex in different cell files. For plastids this is most apparent with respect to the accumulation and loss of starch. Starch is abundant both in the central cells of the rootcap and in cortical cells a short distance above the tip of the root proper but it appears to decline upwards through the root and to be absent from cortical cell plastids in the lateral root zone. Clearly, starch is not always, as is sometimes supposed, a universal constituent of plastids in roots. The plastids of the root hair zone are discoid in shape and have the most extensive (though still limited) thylakoid system so far seen in Phaseolus roots. The plastids of the lateral root zone are spherical in shape and appear to be devoid of thylakoids. If the spatial sequence of plastid development observed as a continuum within the the tip region of the root is continued without interruption into the root hair and lateral root zones, and if this sequence is, as in other organs and in Azolla roots, a direct refiection of an earlier temporal sequence, then both the spherical shape and the scarcity of thylakoids in plastids of the lateral root zone suggest that these plastids have undergone dedifferentiation and lost what internal membrane they had contained during earlier stages of root growth, i.e. that these plastids have regressed from stage 4 to a state resembling stage 1. In roots of P. vulgaris cv. Canadian Wonder grown in soil, membrane-bound bodies were poorly developed compared with those described by Newcomb in roots of the cultivar Dwarf Horticulture grown in nutrient solution in diffuse light. Newcomb suggested that the tubular (thylakoid) complexes and the membranebound bodies might be developmentally linked and that the many invaginations of the inner plastid envelope might also contribute to the formation of membranebound bodies. In the cultivar Canadian Wonder, the membrane-bound bodies were seldom linked to tubular complexes [but see Fig. 3(g)] and invaginations of the inner plastid envelope were comparatively few. However the patterns of distribution within the roots of the two ancillary structures (Figs 4 and 5) would be in general agreement with the concept of their sequential development. When seedlings of P. vulgaris are grown in the dark, plastid development in the root proper, in the hypocotyls and in the primary leaves is always blocked at stage 4 when the plastids lose their pleomorphic shape and the system of single, perforated thylakoids with incipient grana is increasing in extent. However the plastids in the three organs differ considerably in the ancillary structures (like thylakoid complexes) which are produced prior to this stage being reached or at stage 4 itself [Fig. 3(c), (e), (f)]. Many different forms of the tubular or thylakoid complexes have been described in the literature. These complexes show some similarity to, but lack the precise
10 39O J. M. WHATLEY paracrystalline organization of, the prolamellar bodies of leaf etioplasts [Fig. 3(c) to (f)]. Complexes have been observed in many different organs of plants grown both in the light and in the dark. It is sometimes assumed that these various complexes and prolamellar bodies all represent disturbances at different points along the single, tightly-integrated pathway of thylakoid development. The evidence in favour of this assumption is discussed in the recent review by Klein (1982). If the assumption is true, the different forms and relative sizes and rates of development of the various thylakoid complexes and true prolamellar bodies in seedlings of Phaseolus point to a decline downwards through the plant, from the primary leaves towards the root, in the capacity of plastids to produce true prolamellar bodies (and to form thylakoids). In dark-grown seedlings oi Phaseolus this 'gradient' is marked: (1) in the primary leaves, by an extensive and well-organized thylakoid system and by the rapid, uninterrupted production of large paracrystalline prolamellar bodies; (2) in the hypocotyls, by a less extensive thylakoid system and by the much slower production of true prolamellar bodies, a process interrupted, first, by the transitory accumulation of large amounts of phytoferritin, and later, by the transitory formation [Fig. 3(f)] of an unusual thylakoid complex (Whatley, 1978); (3) in the roots, by the production of very few thylakoids and small irregular thylakoid complexes, the latter first appearing as early as stage 1. When seedlings of P. vulgaris grown in the dark for 5 days are exposed to light, the leaves (with true etioplasts) rapidly become green and the hypocotyls (with plastids containing the transitory complex) do so somewhat more slowly. Attempts to induce the roots to green have so far been unsuccessful. These different responses to being transferred from darkness to light by plastids in the three organs appear to reinforce the suggestion that, in adjacent organs of young seedlings, there is a general decline downwards through the plant in the capacity of their plastids to form thylakoids. They also point to the importance (especially in roots) of factors other than light in the control of plastid development. REFERENCES BARLOW, P. W. & GRUNDWAG, M. (1974). The development of amyloplasts in cells of the quiescent centre of Zea roots in response to removal of the root cap. Zeitsckrift fiir Pflanzenphysiologie, 73, BJORN, L. O. (1980). Blue light effects on plastid development in higher plants. In: The Blue Light Syndrome (Ed. by H. Senger), pp Springer-Verlag, Berlin, Heidelberg. ESAU, K. (1965). Plant anatomy. John Wiley and Sons, New York, London, Sydney. ESAU, K. & GILL, R. H. (1973). Correlations in differentiation of protophloem sieve elements in Allium cepa roots. Journal of Ultrastructure Research, 44, GRIFFITHS, H. L. & AUDUS, L, J. (1964). Organelle distribution in the statocyte cells of the tip of Vicia faba in relation to geotropic stimulation. New Phytologist, 63, GUNNING, B. E. S. (1978). Age-related and origin-related control of the number of plasmodesmata in cell walls of developing Azolla roots. Planta, 143, GUNNING, B. E. S., HUGHES, J. E. & HARDHAM, A. R. (1978). Formative and proliferative cell divisions, cell differentiation, and developmental changes in the meristem of Azolla roots. Planta, 143, HELTNE, J. & BONNETT, H. T. (1970). Chloroplast development in isolated roots oi Convolvulus arvensis (L.). Planta, 92, JUNIPER, B. E. & FRENCH, A. (1970). The fine structure of the cells that perceive gravity in the root tip of maize. Planta, 95, KLEIN, S. (1982). Diversity of chloroplast structure. In On the Origins of Chloroplasts (Ed. by J. A. Schiff), pp Elsevier North-Holland, New York.
11 Plastids in roots 391 NEWCOMB, E. H. (1967). Fine structure of protein-storing plastids in bean root tips. Journal of Cell Biology, 33, OLIVEIRA, L. (1982). The development of chloroplasts in root meristematic tissue of Secale cereale L. seedlings. New Phytologist, 91, SALEMA, R. (1971). The production of thylakoids in the roots of a Triticale. Anais de Faculdade de Ciencias {Porto), 54, 1-9. WELLBURN, A. R., ROBINSON, D. C. & WELLBURN, F. A. M. (1982). Chloroplast development in low light-grown barley seedlings. Planta, 154, WHATLEY, J. M. (1977). Variations in the basic pathway of chloroplast development. New Phytologist, 78, 407^20. WHATLEY, J. M. (1978). A suggested cycle of plastid developmental interrelationships. New Phytologist, 80, WHATLEY, J. M. & GUNNING, B. E. S. (1981). Chloroplast development in Azolla roots. New Phytologist, 89,
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