Flora (2002) 197, 224–232 http://www.urbanfischer.de/journals/flora
Stem anatomy of Amaranthaceae: Rayless nature of xylem Kishore S. Rajput Christ College, P. B. No. 5, Saurashtra University P. O., Rajkot 360 005, India e-mail corresponding author:
[email protected] Received: Sept 24, 2001 · Accepted: Feb 6, 2002
Summary Secondary xylem of seventeen species from nine genera of Amaranthaceae was studied anatomically. In all these species radial growth in the main stem was achieved by the formation of cambial variants. After cessation of cell divisions in the previous cambium, a new ring of cambium was developed from axial parenchyma cells at a distance of about three to six cell layers outside the phloem produced by the previous cambium. Among all these species, alternating segments of cambium in each ring led to variation in the differentiation of their derivatives i.e. the segment of cambium producing conducting elements of xylem and phloem (i.e. fascicular segment) and another segment of cambium exclusively producing axial parenchyma cells/conjunctive tissues (interfascicular segment), staggered according to the different cambium rings. In Amaranthus, Celosia and Digera arvensis formation of thick walled xylem derivatives was restricted to the fascicular segment; the interfascicular regions exclusively differentiated into thin walled axial parenchyma cells on both xylem and the phloem side. This variation in the formation of xylem derivatives gives an impression that vascular bundles were embedded in parenchymatous groundmass. In all the other species, the interfascicular regions of the cambium differentiated into thick-walled conjunctive tissues on xylem side and thin walled parenchyma on phloem side. All these species accumulated scanty secondary xylem, which was composed of vessel elements, tracheids, fibres and axial parenchyma while xylem rays were absent at least in the early stages of secondary growth. In the later part of secondary growth, species of Amaranthus, Celosia and Digera arvensis produced axially elongated upright ray cells in the region of cambium that differentiates only into thin walled parenchyma. In the rest of the species xylem was devoid of rays even at the senescent stage of the life cycle. Occurrence of nucleated xylem fibres is an interesting feature of all the species and is correlated with the rayless nature of xylem. Key words: Amaranthaceae, Cambial variants, Rayless xylem, Nucleated fibres.
Introduction Rays play an important role in radial transport of reserve materials, water and storage (Van Bel 1990; Harms & Sauter 1992). Aeration, the radial transport of gases, is also an important function of the rays (Hook et al. 1972; Rajput & Rao 1998a), together with their role in regeneration after wounding (Kuroda & Shimaji 1984; Lev-Yadun & Aloni 1995). An additional function of rays is compartmentalisation from wounding, in which rays participate by forming radial walls of compartments (Shigo 1984). Despite all these roles, a small portion of dicotyledons is devoid of rays (Barghoorn 1941, Gibson 1978; Carlquist 1988; Rao & Rajput 1998 ; Rajput & Rao 1999a, c, 2000). The family Amaranthaceae is well known for its abnormal secondary growth, and this meristem arises from the parenchymatous cells on the periphery of the primary phloem of each vascular bundle. De Bary 224
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(1884) believed it to remain permanently active throughout the life of the plant, but Wilson (1924) considered that it may be constantly renewed in certain (but uncited) examples. Mao (1933) regarded the supernumerary bundles of the family as formed from a continuously active cambium. Schinz (1925), in contrast to this view, believed that the secondary vascular tissue of the stem in the Amaranthaceae is derived from successive cambia of limited activity. Balfour (1965) concluded that the place of initiation of anomalous cambium is found to be variable and it may arise partially from mature cells of the cortex or from meristematic cells. The latter may be in contact with a normal cambium or be situated external to the phloem either in contact with it or quite unconnected with the bundles. Opinions have differed on the mode of formation of secondary growth (De Bary 1884; Dastur 1925; Pfeiffer 1926; Joshi 1937; Metcalfe & Chalk 1950, Lotova & Timonin 1985; Timonin 1987, 1988; 0367-2530/02/197/03-224 $ 15.00/0
Zhang 1989, Rajput & Rao 1999a, c, 2000). In each investigation the attention has been directed mainly on the origin of the meristem responsible for the secondary growth and the way by which it gives rise to secondary tissues. Therefore, all earlier workers have neglected the occurrence of rayless xylem in Amaranthaceae. The present investigation reports on the rayless nature of the xylem and the possible significance of nucleated fibres in seventeen species from nine genera of Amaranthaceae.
Materials and methods Seventeen species from nine genera belonging to Amaranthaceae have been examined anatomically (Table 1). Samples were collected from plants growing at Bhorkheda (North Maharashtra), Pavagadh and Dangs forests of Gujarat State. Eight to ten pieces from the main stems adjacent to ground level were collected from each species and fixed in FAA (Berlyn & Miksche 1976). Suitably trimmed samples were dehydrated through a Tertiary Butanol series and embedded in paraffin. Transverse, radial and tangential longitudinal sec-
Table 1. Dimensional details of fusiform cambial cells, xylem derivatives and length and width of nuclei in the xylem fibres (in µm) in the investigated members of Amaranthaceae Sr. No
Name
Fusiform cambial cell length
Vessel Element Length Width
Xylem Fibre Length Width
Fibre Nuclei Length Width
1.
Amaranthus spinosus Linn.
148 ± 3.77
135 ± 3.51
55 ± 1.28
434 ± 6.75
16 ±1.67
4 0.61
3 0.32
2.
Amaranthus paniculatus Linn.
188 ± 3.10
142 ± 4.91
65 ± 1.21
545 ± 6.01
20 ± 2.06
6 0.61
3 0.39
3.
Amaranthus viridis Linn.
169 ± 3.77
148 ± 3.78
53 ± 1.42
415 ± 6.43
17 ± 1.87
7 0.79
4 0.57
4.
Amaranthus polygamus Linn.
175 ± 4.69
160 ± 4.44
60 ± 1.47
460 ± 5.98
16 ± 2.03
5 1.20
2 0.86
5.
Amaranthus lividus Linn.
155 ± 3.41
130 ± 2.29
55 ± 1.34
480 ± 6.50
19 ± 2.38
7 1.92
4 0.39
6.
Amaranthus tenuifolius Willd.
175 ± 4.21
157 ± 2.44
60 ± 1.49
530 ± 7.02
20 ± 1.43
6 0.98
3 0.68
7.
Aerva lanata Juss.
154 ± 4.24
138 ± 3.29
53 ± 1.68
485 ± 7.51
18 ± 0.99
5 1.01
3 0.41
8.
Celosia polygonoides Retz.
142 ± 5.07
128 ±2.98
49 ±1.98
476 ± 6.36
21 ± 1.54
7 0.79
3 0.49
9.
Celosia cristata Linn.
174 ± 4.73
159 ± 2.83
68 ± 1.28
675 ± 8.76
21 ± 1.53
6 1.21
3 0.31
10. Celosia pulchella Moq.
182 ± 4.88
173 ± 3.18
64 ± 1.34
669 ± 7.41
19 ± 1.62
7 0.62
4 0.59
11. Digera arvensis Forsk.
178 ± 5.37
146 ± 3.48
72 ± 1.29
655 ± 7.33
20 ± 1.35
6 0.89
3 0.40
12. Gomphrena globosa Linn.
165 ± 4.77
135 ± 2.96
67 ± 1.59
598 ± 6.64
17 ± 1.25
5 0.38
3 0.57
13. Gomphrena celosioides Mart.
152 ± 5.34
129 ± 2.68
57 ± 1.87
517 ± 5.98
16 ± 1.10
4 0.73
3 0.51
14. Nothosaerua brachiata Wight
157 ± 5.23
132 ± 3.69
63 ± 1.45
512 ± 7.43
19 ± 1.71
5 0.92
3 0.41
15. Telanthera ficoidae Moq.
173 ± 4.54
164 ± 3.12
59 ± 1.98
632 ± 8.91
17 ± 0.99
6 1.08
2 0.61
16. Pupalia atropurpurea Moq.
198 ± 4.66
175 ± 2.73
69 ± 2.04
794 ± 5.79
18 ± 1.32
9 1.55
4 0.32
17. Cyathula prostrata Blume
149 ± 5.27
127 ± 2.79
61 ± 2.09
578 ± 6.43
20 ± 2.03
7 1.36
4 1.03
FLORA (2002) 197
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tions, 15–20 µm thick, were obtained with a rotary and sliding microtome and stained with a safranin-fast green combination for general studies. Some of the sections were also stained with 4% acetocarmine and I2KI for nucleus and starch localisation respectively. Maceration of xylem of each species was also prepared to study general morphology and size of vessel elements and fibres. One hundred measurements were chosen randomly to obtain mean and standard deviation.
Results All the species studied are annual, erect and much branched herbs reaching 0.4 to 1.5 m in height. Amaranthus paniculatus, A. polygamus, Celosia cristata, Gomphrena globosa and Telanthera ficoidea are cultivated species while the other taxa are growing wild in wastelands and forest areas. Stem diameter varies from species to species ranging from 10 – 25 mm.
Structure of vascular cambium The stem is composed of three to five successive cambium rings composed entirely of fusiform cambial initials. But in the later part of secondary growth, in Amaranthus, Celosia and Digera arvensis some of the fusiform cambial cells undergo further division and result in the development of vertically elongated rays. The cambium consists of relatively short fusiform cambial cells varying from 142 –198 µm in length. In transverse view, the cambium appears to be two to three layered when non-dividing, and four to six layered during the development of xylem and phloem. Functionally each cambium is divided into two distinct types: i) the region of cambium producing conducting elements of xylem and phloem, and ii) the region of cambium producing thick-walled conjunctive tissues toward the xylem in Gomphrena, Nothosaerua, Pupalia, Cyathula and Telanthera or thin walled conjunctive tissues on both xylem and phloem side in Amaranthus, Celosia and Digera arvensis.
Development of vascular cambium In all the species studied, the first ring of cambium ceases to divide after a limited period of activity and the second ring of cambium develops from the axial parenchyma cells at a distance of about three to six cell layers outside the phloem produced by the previous cambium (Fig. 1 A). During the development of new cambium one or two parenchyma layers undergo repeated periclinal divisions and result in the formation of a band of cells (cambium) three to four cells wide arranged in radial 226
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files. The four to five layers of parenchyma between the newly developed cambium and the phloem produced by the previous cambium differentiate into conjunctive tissues (Fig. 1A, B). The formation of subsequent cambia follows a similar pattern of development. In some of the species like Pupalia atropurpurea, Telanthera ficoidae, Cyathula prostrata, Nothosaerua brachiata and in both species of Gomphrena, development of a new cambium ring is observed only after the cessation of cell divisions in the previous cambium (Fig. 1C) while in all species of Amaranthus development of new cambium is seen even though the previous cambium is still functionally active and giving rise to xylem and phloem elements (Fig 1A, D). As aforementioned, the cambium of Amaranthus, Celosia and Digera species is functionally separated into two distinct types producing thin walled conjunctive elements on either side of cambium while development of thick walled xylem elements is restricted to certain portions of the cambium (Figs. lA, 2A). By this way vascular elements are formed patchily by the cambium so that the vascular bundles are embedded in a parenchymatous groundmass (Fig. 2A). In the other species the cambium is functionally also of two types, but conjunctive tissues produced towards the xylem side are always thick-walled and lignified. This variation in vascular element differentiation results in a formation of successive rings of thick-walled xylem alternating with rings of thin-walled parenchyma and sieve elements (Figs. 1A, 2D and 3A, B). Unlike Pupalia and Aerva (Figs. 2D and 3B) the rings of thick walled xylem derivatives and thin walled parenchyma cells and sieve elements are not continuous in Gomphrena (Fig. 3A). But they are discontinuous and anastomosing in Gomphrena due to the renewal of cambium in small segments, whereas in Pupalia and Aerva the entire ring of cambium ceases to divide at a time and a complete new ring is formed. A similar feature has also been observed in the species of Amaranthus (Fig. 2A).
Structure of xylem In the mature stem of all species studied in the present investigation, xylem is composed of vessel elements, tracheids and fibres while xylem rays are absent at least in the early stages of xylem development (Figs. 2A, B, D; 3A, B). In the species of Amaranthus, Celosia and Digera, during the latter part of the secondary growth (when these plants attain their reproductive stage), the axial parenchyma produced from the relatively wider segment of cambium undergoes further divisions resulting in the formation of vertically elongated upright rays (Fig. 2A–C). These rays are uniseriate to multiseriate (i.e. several cell files in width). Thus, many rays have
Fig. l. Transverse (A–F) sections of cambium and xylem of Amaranthus, Pupalia and Digera arvensis. A: Development of new cambium in A. paniculatus (broad arrows). The parenchyma between newly developed cambium and phloem from previous cambium differentiate into conjunctive tissues (small arrow). Arrowheads indicate differentiating vessel elements. B: Newly developed cambium with few differentiated xylem derivatives in A. spinosus. Arrow indicates the parenchyma, which differentiates into the conjunctive tissue. C: Development of new cambium after the cessation of cell divisions in previous cambium in Pupalia (arrows). Arrowheads indicate complete differentiation of previous cambium. D: Development of new cambium in A. paniculatus (arrows) even though the previous cambium is functionally active. Note the differentiating unlignified vessel elements in A. paniculatus (arrowheads). E: Xylem structure of Digera arvensis. Arrowheads show thinwalled parenchyma cells formed on either side of the cambium. F: Xylem structure of Pupalia atropurpurea. Note the thickwalled derivatives on xylem side (arrowhead). Fig. 1A–C: Scale bar =75 µm, Fig. 1D–F: Scale bar = 100 µm. FLORA (2002) 197
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Fig. 2. Transverse (A, D) and tangential longitudinal (B, C) xylem sections of Amaranthus spinosus, A. paniculatus and Pupalia atropurpurea. A: Xylem structure of Amaranthus spinosus before the formation of rays. Note the variation in the formation of xylem derivatives (i.e. thick walled conducting elements restricted to certain portions of the cross section). B: Absence of rays in Amaranthus paniculatus during the early stages of secondary growth. The left side shows thick walled elements, the right side thin walled conjunctive tissues. C: Amaranthus paniculatus showing well developed axially upright rays (arrows) in the later stage of secondary growth. D: A stem showing discontinuous successive rings of xylem in Pupalia atropurpurea. Note the difference in xylem structure when compared with that of Amaranthus spinosus. Fig. 2A–D: Scale bar = 225 µm. 228
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Fig. 3. Transverse (A–B) and tangential longitudinal (C–E) sections of xylem in Gomphrena, Aerva, Cyathula, Nothosaerua and Telanthera. A: Stem of Gomphrena globosa showing overlapping rings of secondary xylem. B: Stem of Aerva lanata showing radial multiples of vessels and successive rings of xylem alternating with phloem bands. C: Xylem showing only axial elements in Cyathula prostrata. Note the elongation of cell tips, thus becoming non-storied. D: Rayless xylem of Nothosaerua brachiata. E: Xylem showing absence of rays in Telanthera ficoidae. Fig. 3A–E: Scale bar = 225 µm. FLORA (2002) 197
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upright cells at their tips. Like fusiform cambial cells xylem fibres, tracheids and axial parenchyma are arranged in a storied fashion (Fig. 2 B and 3C–E). In all these members of Amaranthaceae, development of conducting elements of xylem and phloem is confined to a certain portion of cambial segments (Fig. 2A). This leads to the development of vessels mostly in radial multiples of 2–6 cells (Fig. 3A, B). They have simple perforation plates, with alternate bordered pits on their lateral walls. The average length and width of vessel elements differed from species to species. The greatest values were observed in Pupalia atropurpurea (175 µm) and Digera arvensis (72 µm) and the least ones in Cyathula prostrata (127 µm) and Celosia polygonoides (49 µm), respectively (Table 1). Xylem fibres in all the species retained their living protoplast even after the deposition of secondary wall material. The length of nuclei including sharp points varied from 4 µm in Amaranthus spinosus to 9 µm in Pupalia atropurpurea. Morphologically, xylem fibres vary greatly among all the species; some of the fibres are straight and spindle shaped while others have undulating walls. Occurrence of branched fibres is a common feature in all the plants. Pits on the walls are simple and confined to radial walls. Their slit-like aperture forms a narrow angle with the fibre axis. The length of fibres varies from species to species and ranges from 794 µm in Pupalia atropurpurea to 415 µm in Amaranthus viridis. Their lumen diameters differ from species to species and are relatively wide (21 µm) in Celosia cristata and Celosia polygonoides (Table 1). Accumulation of starch in the fibre lumen is a characteristic feature of all the species studied.
Discussion The pattern of secondary growth in Amaranthaceae differs from that of many dicotyledons (Balfour 1965; Fahn & Zimmermann 1982). As reported by earlier workers (Balfour 1965; Philipson & Ward 1965; Baird & Blackwell 1980; Fahn & Zimmermann 1982 ; Lotova & Timonin 1985; Timonin 1987, 1988; Zhang 1989 ; Rajput & Rao 1999a) development of successive cambia takes place from the outermost phloem parenchyma cells in all the species studied. However, much attention has been paid to the question of whether each growth increment of secondary vascular tissue arises from a separate cambium layer or from a residuum of the previous cambium (Balfour 1965; Philipson & Ward 1965; Baird & Blackwell 1980; Fahn & Zimmermann 1982), while composition and development of their derivative tissues remained neglected (Rao & Rajput 1998; Rajput & Rao 1998b; 1999 a). De Bary (1884) and Balfour (1965) have 230
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studied the development of a secondary meristem thoroughly in Celosia argentea and Celosia thompsoni, but there is no mention of the absence of a radial system in xylem and phloem in the early part of secondary growth and the occurrence of nucleated xylem fibres. Raylessness tends to occur in plants with limited cambial activity and results in a scanty accumulation of secondary xylem (Carlquist 1970). But sometimes it may be seen in plants with considerable thick stems as observed in Bougainvillea. lf a single cambium can no longer produce more xylem, then successive cambia may increase stem or root diameter. Such a xylem always remains rayless as it was noted by Barghoorn (1941), Carlquist (1970), Rao & Rajput (1998), and Rajput & Rao (1 998b, 1999a). However, in the present investigation all the studied species of Amaranthaceae show a scanty accumulation of secondary xylem by the formation of successive cambia. All the studied Amaranthaceae are ephemeral herbs, reaching 45 to 60 cm in height. They complete their life cycle before the seasonal arrival of dry conditions (i.e. from June to December or January). Under these circumstances, the secondary xylem cylinder never becomes thick enough for the development of rays. As compared with the other studied taxa Amaranthus, Celosia and Digera arvensis grow up to late summer (i.e. from June to April–May) and they become taller than other plants. Thus, their height and the relatively longer life span may be responsible for the formation of rays at the end of their life cycle. Absence of rays is not a common feature and is restricted to a few species of dicotyledons belonging to quite different families (Carlquist 1988; Lev-Yadun & Aloni 1995; Rao & Rajput 1998; Rajput & Rao 1998b, 1999a). I add here a few more species belonging to the family Amaranthaceae to the list of plants with rayless xylem, which has not been reported earlier. However, rays if produced in species with principally rayless xylem occur only in the outer portion of the secondary xylem, as noted by Barghoorn (1941) for Geranium tridens, for Plantago webbii by Carlquist (1988) and for Suaeda monoica by Lev-Yadun and Aloni (1991). Such rays are shown here for the species of Amaranthus, Celosia and Digera arvensis. Ray initials were eliminated from the cambium of Glycine max following 2,4-DB application (Pizzolato 1982). Thus, changes in hormonal stimulation are probably involved in the transition from a juvenile rayless stage to a mature wood containing rays in plants, which display juvenile raylessness (Lev-Yadun & Aloni 1991). The phenomenon of initiation of vascular rays in the mature parts of the temporary rayless wood, as observed in Amaranthus, Celosia and Digera arvensis, is already known in other species (Barghoorn 1941; Carlquist 1988; Lev-Yadun & Aloni 1991).
Lev-Yadun & Aloni (1991) suggested that this aspect of ray initiation and development is a specific case of a more general phenomenon of the gradual initiation and increase in ray size following maturation of wood in plants. This general pattern of an increase in the size of rays, vessels, tracheids and fibres is correlated with age and distance from the stem apex of the plant (Aloni & Zimmermann 1983; Saks & Aloni 1985; Bhat et al., 1989 ; Lev-Yadun & Aloni 1991). This gradient in the dimensions in the vascular elements and fibres have been explained by a decreasing gradient of auxin concentration from leaves to roots (Aloni & Zimmermann 1983 ; Aloni 1987, 1991). lt has been proposed that the regulation of ray size is influenced by a decrease in auxin level from leaves to roots (Lev-Yadun & Aloni 1991). The decrease in axial polar auxin flow from leaves to roots results in a relative increase in the effect of radial signal flow, which may be responsible for the development of rays in temporary rayless plants. One of the evolutionary trends found in cambial activity is to result in herbaceous plants type. When secondary woodiness develops the fusiform cambial cells are very short and give rise to highly specialized cell types in the secondary xylem (Gibson 1978). Similar trends were found in all species used in the present study. The occurrence of nucleated xylem fibres seems to be associated with the rayless nature of xylem. Fahn & Leshem (1963) considered that nucleated xylem fibres are an adaptive feature, associated with the diminishing supportive function, exhibiting a transition towards parenchyma cells that prevail in herbaceous plants. Moreover, accumulation of starch in these fibres also suggests that in addition to mechanical support they also act as a reservoir of photosynthetic products representing a further functional connection between parenchyma cells and wood fibres (Rajput & Rao 1999b, c). Parameshwaran & Liese (1969) correlated the ability of xylem fibres to accumulate starch with paucity of storage parenchyma. The presence of nucleated xylem fibres suggests that these fibres may not only act as a reservoir of photosynthate but also play an important role in radial conduction.
Acknowledgement The author is thankful to both the anonymous referees for their critical suggestions and the improvement of the manuscript.
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