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First published online October 8, 2008; doi:10.3732/ajb.0800083 American Journal of Botany 95: 1337-1348 (2008) © 2008 Botanical Society of America, Inc. |
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Anatomy and Morphology |
Fairchild Tropical Botanic Garden 11935 Old Cutler Road, Coral Gables, Florida 33156 USA
Received for publication 29 February 2008. Accepted for publication 14 August 2008.
ABSTRACT
The hypocotyls or roots of many seed plants contract during seedling growth. Anatomical evidence is here reported for the first time that G-fibers (gelatinous or tension wood fibers) may cause contraction of roots and hypocotyls in dicotyledonous seedlings long after germination. To document repositioning of seedling buds, selected perennials (20 dicotyledons and one cycad) native to the fire-prone pine rocklands of subtropical South Florida were germinated and measured for 4–5 mo. The height of cotyledonary nodes above the soil decreased because of axis contraction or bending in eight species. Anatomy suggested that two mechanisms operate: (1) previously well-documented collapse of parenchyma cells in two species (Convolvulaceae and Zamiaceae) and (2) newly documented production of G-fibers in six species (all Fabaceae). Contraction or bending of the hypocotyl and/or taproot moved the cotyledonary and later buds of the seedling closer to the soil surface or buried them. Bud repositioning by these mechanisms may protect the lateral buds from injury by fire or other environmental stresses and allow resprouting.
Key Words: contractile root • fire adaptation • gelatinous fiber • hypocotyl • reaction wood • seedling • tension wood
Contractile roots appear to be adaptive in repositioning perennating buds below ground in many plant communities exposed to environmental stresses such as fire, seasonal drought, severe freezing and soil heaving due to frost (Pütz, 2002
). The shoots of seedlings and sometimes adults are pulled deeper into the soil, thus offering buds greater protection. Although not widely appreciated, seedling axis contraction in dicots has been well documented. Rimbach (1926, 1929) listed a variety of dicots, in addition to monocots and cycads, that showed axis shortening over time. However, he gave no indication of the anatomy of these species, and since then, there have been reports of root shortening in dicots but relatively few anatomical studies of this phenomenon.
In the pine rockland plant community of subtropical South Florida, periodic fires historically maintained a savanna-like habitat with an overstory of slash pine (Pinus elliottii var. densa Little & Dorman) and an understory of saw palmetto [Serenoa repens (Bartram) Small], woody shrubs, and herbs (Snyder et al., 1990). Fire-prone Florida communities are rich in long-lived herbaceous and small woody perennial dicot species that can survive fire by resprouting or, in some cases, germinating from a seed bank (Menges and Kohfeldt, 1995). The majority of woody perennial species in pine rockland resprout after fire, although the exact percentage has not been published. Because frost is rare in this subtropical environment, regeneration after fire is a likely strong selective factor for seedlings.
In the small shrub, Amorpha crenulata Rydb., I observed the wrinkled surface of thickened taproots that was suggestive of a contraction of the taproot in seedlings and old plants. Previously, Stevenson (1980) described contractile roots and stems of Zamia pumila L., a native cycad from this same habitat. Additionally, the roots of Amorpha had G-fibers (= gelatinous or tension wood fibers) in which the inner secondary cell walls are unlignified; composed of cellulose, pectin, and arabinogalactan proteins (Bowling and Vaughn, 2008); and easily recognized in transverse sections. The G-fibers in Amorpha suggested a contraction of the taproot similar to aerial roots of Ficus that contract when G-fibers are produced after anchoring of the root in the ground (Zimmermann, et al., 1968). Significantly, root contraction in other flowering plants has never before been associated with G-fibers, and fibers are absent in contractile roots of Zamia. G-fibers are commonly found in upper sides of woody branches and leaning trunks of dicot trees. There is evidence that the production of G-fibers increases tensile forces in wood and can result in a bending or longitudinal shortening of the axis (Zimmermann et al., 1968; also see citations in the Discussion). The original observation of Amorpha led to a survey of other perennial species for evidence of seedling contraction that might pull the cotyledonary buds deeper into the soil during the normal germination process and for the role G-fibers play in this process.
The role of fibers in seedling axis shortening would be a new mechanism for seedling root contraction. The well-studied mechanism for contractile roots of monocots involves collapse of vascular and cortical parenchyma cells (reviewed by Pütz, 1999, 2002). In taproots of cycads (Stevenson, 1980) and adventitious roots of numerous monocotyledons (Jernstedt, 1984; Pütz, 1999, 2002; Ruzin, 1979; Wilson and Anderson, 1979), anatomical features that might account for organ shortening were the reorientation of growth and longitudinal collapse of cortical parenchyma cells. Do dicot roots contract by the same parenchyma mediated mechanism as in monocot roots or do G-fibers play a role?
Among dicots, Oxalis is a classic example of root shortening in a dicot, and its morphology and biomechanics were described but not its anatomical mechanism (Pütz, 1994). In an ephemeral desert annual species of Asteraceae, Zamski et al. (1983) found that the seedling taproot contracted by means of decreased cell length in the fleshy pericycle and primary phloem, similar to the monocot roots noted. Pütz and Sukkau (1995, 2002) documented the amount of contraction in taproots of various Apiaceae but did not directly relate their finding to anatomy. Pütz (2006, p. 302) measured seedling displacement in a species each of Rosaceae and Asteraceae, but again presented no anatomical information, although he noted "in most dicots external contraction features are missing (e.g., shrinkage of the root surface in monocots). Therefore, contraction phenomena in dicots are only visible by anatomical studies." The preliminary observation on G-fibers in Amorpha roots points to a new and different anatomical mechanism for root contraction. The current study seeks to remedy this lack of information about the mechanisms of hypocotyl and root contraction in dicots. It will also document a strategy for plant survival in this fire prone habitat.
MATERIALS AND METHODS
A selection of perennial species common in the pine rockland community of South Florida (listed in Table 1) was constrained by seed available from wild and cultivated plants. This represents roughly 20% of some 100 species of woody dicot perennials (trees, shrubs and vines) that are native to the pine rockland according to the Institute for Regional Conservation (http://regionalconservation.org/ircs/database/plants/ByHabitat.asp?HabCode=PIR&Habitat=Pine%20Rockland). After being surface sterilized with sodium hypochlorite solution, seeds were sown in plastic Petri dishes filled with washed quartz sand. Germinated seeds with a radicle or cotyledon were transplanted into 5 x 18 cm plastic pots (D40 Deepots, Stuewe & Sons, Corvallis, Oregon, USA) each filled with 470 cm2 of a mix of 1:1 potting soil and local limestone gravel (sieved at 1 cm). For each species, 10–11 replicate pots with one seedling each were watered and lightly fertilized as needed and grown on benches in a glasshouse under ca. 50% shade. Measurement began after the seedling was well rooted and the hypocotyl (if present) or the first internode stopped elongating. Direct measurements were made in reference to a metal bar laid across the top rim of the pot. Soil level was noted by embedding a stainless steel bolt nut into the medium and measuring the distance from the nut to the bar. The distances of the cotyledonary node and sometimes the next distal node were measured from the metal bar to the nearest 0.5 mm directly with a ruler every 4 wk. Changes in the depth of the cotyledonary node were always related to the steel nut to account for possible soil compaction or expansion during seedling growth. Some measuring error was caused by different positions of the metal bar on the pot rim, but this appeared to be no more than ±1 mm. In some species, one or more seedlings died or were unhealthy (see N noted in Table 1) and were omitted from calculations.
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). Sections were photographed with a Nikon Coolpix 4500 camera (Nikon, Tokyo, Japan) on a Leitz Ortholux 2 (Wetzlar, Germany) microscope. Anatomical observations were made on at least three different seedlings of each species used in the growth measurements.
RESULTS
Growth measurements
The height of the cotyledonary node either remained unchanged or decreased during 4–5 mo of measurements. For convenience, only the genus name will be used in comparing species except for Senna, in which two species were examined. The complete nomenclature is given in Table 1.
Noncontractile seedlings
The position of the cotyledonary node remained essentially unchanged for 13 species; mean final height varied by less than 2 mm from the original height in relation to the soil level (Table 1, Fig. 1). The month to month variation in heights was mainly due to measurement error as noted and oscillated around zero, in contrast to the obvious decrease in height observed in eight species (Fig. 2). Replicate seedlings also varied in their general vigor and plant size. Average height of cotyledonary nodes increased by more than 1 mm in Forestiera and Sida, presumably due to prolonged primary elongation of the hypocotyls after the start of measurements. Average height of Sophora (Fig. 3D) decreased by 1.6 mm (Table 1) and suggested a tendency for some contraction as noted later. All seedlings had a well-developed taproot (Fig. 3) except for Passiflora, that had a fibrous root system directly below the hypocotyl. The cotyledonary node remained at or within a few millimeters from soil level only in those species having little or no hypocotyl elongation (Byrsonima, Jacquemontia, Fig. 3A; Lantana, Passiflora, Pithecellobium, Fig. 3C; Psidium, Sophora, Fig. 3D), Tetrazygia). Species that initially raised and maintained their cotyledonary bud 10 mm or more above the soil were Forestiera, Morinda, Rhus, Senna ligustrina (Fig. 3B), and Sida. There were no surface wrinkles, although the periderm was rough and longitudinally split in some hypocotyls.
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Noncontractile seedlings
Generally, stems were woody with lignified secondary xylem. Hypocotyls had a similar stem-like organization (Fig. 5A, D) with a decrease in pith area toward the root end. Roots typically lacked a pith, although some species had a central nonvascular medulla (Forestiera, Morinda, Pithecellobium). Xylem fibers were all normal in the hypocotyls and roots of Jacquemontia (Figs. 3A, 5B, C) and Forestiera (Fig. 5E, F) and others (see Table 1). Starch-filled parenchyma was common in the pith, xylem (Fig. 5F), phloem, and cortex, especially in roots.
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The hypocotyls and roots of some species contained G-fibers, which were defined by thick, glistening inner walls in thick sections (Fig. 7H). In thinner sections, the clearly unlignified inner walls were stained pink-purple with toluidine blue (Fig. 5K, N) or light pink to clear with phloroglucinol (Fig. 5L, O), and very narrow lumens in hydrated sections. Scattered arcs and clusters of G-fibers were found in xylem of Passiflora, Pithecellobium, and Rhus. Scattered G-fibers occurred mainly in the phloem of Senna and Sophora. The well-developed G-fibers in the phloem of Sophora (Figs. 3D, 5G–I) were correlated with the slight contraction observed in this species.
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Contractile seedlings with parenchyma collapse
Two species had swollen, succulent hypocotyls and taproots and no evidence of G-fibers (only normal fibers in Ipomoea and tracheids in Zamia). In Ipomoea, the hypocotyl was succulent (Figs. 4E, F, 6A). The parenchyma cells were radially elongated in the xylem, some cells were collapsed in the axis center, and cells were radially stretched in the cortex adjacent to the wrinkled periderm (Fig. 6B). The older wrinkled hypocotyl (Fig. 4E, F) had convoluted periderm and outer cortex as seen in longitudinal section. Xylem parenchyma were radially enlarged as seen in transverse section (Fig. 6E–H) compared to the same tissues in the younger smooth root (Fig. 6A–D) 20 mm distant from the same hypocotyl. Vascular bundles in the wrinkled region of the hypocotyl (Fig. 6K, L) were more irregular than those in the smooth region of the root (Fig. 6I, J), evidence of longitudinal shrinkage. Presumably, the young smooth root would have developed the features of the wrinkled hypocotyl as the wave of contraction spread from hypocotyl to root.
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Evidence of cortical cell enlargement and collapse was found in wrinkled hypocotyls of Amorpha, Dalea, Galactia, and possibly Tephrosia. However, it was uncertain if parenchyma cell distortions were the result or the cause of root contraction.
Axis bending in Senna mexicana
Although the germinated seeds were transplanted with the epicotyl in the upright position, the more or less vertical hypocotyl and lower stem region became reoriented to the horizontal position (Figs. 4G, 7A, B). The base of the stem became swollen at and below the cotyledonary node, with increased swelling in the hypocotyl and root. At 5 months after germination, the two to three internodes above the cotyledonary node were slightly oblique to the vertical. The stem had little secondary xylem with mostly normal fibers or fibers with intermediate structure in which thick inner walls had less lignin staining and fibers had a less angular shape than normal fibers (cf. Fig. 7D and G). Closer to the cotyledonary node, there were few to many G-fibers in the xylem, depending upon the level of section. The outer phloem had a continuous band of G-fibers at the cortex boundary. The vertical internode directly above the cotyledonary node (= internode 1) had well-developed secondary xylem: up to six to seven times more than internode 2 or 3. Although the axis was slightly oblique, the xylem was either concentric or slightly eccentric, with more on the upper side. The G-fibers in the phloem were dispersed due to the wider axis. In the curved part of the hypocotyl, the secondary xylem was very eccentric with two to three times as much xylem on the lower side (or inner side of the bend, Fig.7H) compared to the upper (or outer) side (Fig. 7E). There was more xylem parenchyma in the hypocotyl than in the stem, and rays were wider on the upper side than on the lower side of the hypocotyl. Some normal fibers (or intermediates between G- and normal fibers in the amount of inner wall lignification) were present in arcs or bands on the upper side, with only normal fibers near the cambium in this sector (Fig. 7F, G). On the inner (lower) side, the xylem had mostly G-fibers with a clear distinction between a thick unlignified inner secondary wall layer and a thin lignified outer wall layer (Fig. 7I–K). The inner wall was swollen in aqueous preparations with little or no lumen visible. The distinction between inner and outer wall layers was more distinct in thick sections with toluidine blue when the inner wall layer was either clear and bright (Fig. 7K) or pink (Fig. 7I) in thin sections stained with toluidine blue. The root contained mainly G-fibers.
DISCUSSION
Mechanism of axis contraction
Nearly half the species examined had measurable contraction of the seedling axis (hypocotyl and root). Two mechanisms for contraction are suggested by the anatomy of the seedlings: (1) production of G-fibers, which have a strong phylogenetic association (family Fabaceae); and (2) collapse of parenchyma cells.
Axis contraction is correlated with the presence of G-fibers (= tension or reaction wood fibers) in the hypocotyls and roots in six species of Fabaceae (Table 1). Since G-fibers are produced in leaning or displaced dicotyledonous stems (Fisher, 1985; Patten et al., 2007) and are associated with increased tension forces in the wood (Bamber, 2001; Yamamoto et al., 2005) and the movement of stems back to their normal orientation (Fisher and Stevenson, 1981), the symmetrical production of G-fibers is the probable cause of the axis contraction observed in seedlings from the pine rockland. Symmetrical production of G-fibers was documented in aerial roots of Ficus and occurred only after the formation of G-fibers (Zimmermann et al., 1968). G-fibers also occurred in aerial roots of other Ficus species and Cecropia (Fisher, 1982).
Many trees, especially Fabaceae, have G-fibers in their roots, either on the lower side in horizontal roots or at various positions in vertical roots (Patel, 1964). In Robinia, G-fibers were most common in the first-formed xylem near the center, i.e., in the young root (Patel, 1964). The presence of G-fibers was widely distributed among dicot roots (Höster and Liese, 1966) and was found in some of the families represented in the current study (Fabaceae and Anacardiaceae, but not Passifloraceae). Unfortunately, in the detailed studies of root contraction in seedlings of a number of species of Apiaceae (Pütz and Sukkau, 2002; Pütz 2006), neither root anatomy nor the type of fibers were described.
Seedlings of other species of Fabaceae show hypocotyl or root contraction. In Melilotus, only "fibers" were described in the shortened hypocotyl (Bottum, 1941). The shortening of Lotononis hypocotyl was promoted by high light levels (Fujita and Humphreys, 1992), but again anatomy was not examined. The seedling taproot of Trifolium shortened and "fibers" were mentioned, implying normal fibers (Cresswell et al., 1999). These authors suggested a mechanism for axis shortening by the transverse spreading of the phloem fiber strands via parenchyma enlargement. A similar mechanism for erection of displaced Ochroma and Carica stems was proposed by Fisher and Mueller (1983), but this is not suggested by the present observations of seedling anatomy. Recently, G-fibers were described in both the phloem and xylem of young branches of Medicago (Patten et al., 2007), but changes in internode length were not investigated.
In the current study, G-fibers were not always associated with contraction, but the degree of G-fiber production was related to contraction or bending. Scattered xylem and phloem G-fibers were found in several noncontractile species (Table 1). Senna ligustrina had G-fibers in the phloem, but without axis contraction, while S. mexicana had more G-fibers in the phloem and xylem and showed hypocotyl bending on the side with the greatest number of G-fibers. Sophora had some G-fibers, especially in the phloem and was questionably contractile, further indicating that the degree of contraction may be variable and related to amount and distribution of G-fibers. Clearly, all Fabaceae species with axis contraction or bending had well-developed G-fibers.
The progressive bending of the hypocotyls in Senna mexicana was correlated with the asymmetrical production of xylem with G-fibers on the lower side of the axis. Total number of G-fibers was greatest on the lower or inner side of the bend, again correlated with the region of contraction and in a position noted for reaction wood in some dicotyledon roots (Patel, 1964). Tension wood (= G-fibers) was most commonly found on the upper side of stems and branches of dicotyledons or in a less patterned, spiral arrangement in branches of an herbaceous Fabaceae (Patten et al., 2007). However, there were reports of tension wood formed on the lower side of lateral branches of dicots, followed by a shift in tension wood production to the upper side that was a part of the normal ontogeny in trees with particular architecture (Fisher and Stevenson, 1981). Hypocotyl bending in S. mexicana may be caused by a randomly positioned imbalance in the number of G-fibers in the hypocotyl that causes an initial displacement of the hypocotyl. Once this small reorientation occurs, the lower side is stimulated to produce more secondary xylem and hence more G-fibers, which in turn increases the tension of the lower side (now the inner side of the bend) and promotes the bending of the hypocotyl. G-fibers also occur in Senna ligustrina, but presumably any resulting tension was neither sufficient to cause measurable contraction nor asymmetrical enough to cause axis bending.
Two species (Ipomoea and Zamia) displayed contraction, but lacked G-fibers. In the presumed region of contraction (= wrinkled surface), the parenchyma cells enlarged in the radial direction and had regions of collapse. The increased irregularity of central vascular bundles in this region was strong evidence for longitudinal shrinkage and distortions in the center of the axis. Stevenson (1980) described radial plates of tissue collapse and distortion of the stele in fleshy stems of Zamia that were older and larger than those observed in the current study. Similar descriptions of radial expansion and longitudinal shortening of cortex cells in contractile primary roots of monocots indicated a similar involvement of cortical parenchyma (Ruzin, 1979; Jernstedt, 1984; Pütz, 1999). However, these authors found no evidence of stele distortion in contracted roots, as described for Ipomoea and Zamia. Some evidence of cell enlargement and collapse in the outer cortex was found in Amorpha, Dalea, Galactia, and perhaps Tephrosia, where G-fibers also develop. It was possible that the cortex in these species collapsed as a consequence of contraction or that they had two mechanisms for contraction: radial cell enlargement and G-fibers. Clearly, we need further detailed anatomical and experimental studies on these two presumed anatomical mechanisms in one or more selected species.
Ecological significance
Studies of other fire-prone communities classified two major types of plant regeneration responses or strategies after fire: reseeding and reprouting (Pate et al., 1990, 1991; Bellingham and Sparrow, 2000; Ojeda et al., 2005). The new shoots in resprouters arise from "rootstocks," rhizomes, lignotubers, or more rarely root suckers (Gill, 1981), but are often described without anatomical details that would explain the origin of these new shoots. It was assumed that regeneration arose from dormant lateral buds of the cotyledons and lowest nodes of the shoot. Shoot damage due to freezing is less frequent than to fire in the subtropical pine rockland. From a global viewpoint, persistence of damaged plants by resprouting is a significant aspect of their life history and may relate to the limited seedling recruitment observed in many of these species (Snyder, 1986; Snyder et al., 1990; Bond and Midgley, 2001). Indeed, the fact that many fire-adapted species persist rather than recruit as a life strategy was emphasized by Bond and Midgley (2001). All 21 seedlings examined are resprouters, although Passiflora may be most susceptible to fire damage, and all except Lantana, Passiflora, and Senna ligustrina are long-lived (Table 1).
Fire-adapted plants that resprout have buds positioned at or below ground level. Because these plants are usually old woody perennials, the morphology and origin of these basal regenerating buds are often obscure. Some may be dormant axillary (lateral) buds, and some may be adventitious in origin (arising from the vascular cambium of the shoot or the root). Buried seeds that are hypogeal keep their cotyledons and the cotyledonary and some subsequent nodes at or below ground level (Ipomoea, Pithecellobium, Sophora, Zamia).
A number of savanna species from a range of families had seeds and fruits that germinated at the soil surface but buried their plumules (= cotyledonary node), termed "cryptogeal germination" (Jackson, 1974). essentially the same as "remote epigeal germination" in palms and cycads (Tomlinson, 1990; Henderson, 2006). The embryo is pushed out of the seed coat and some distance away from the seed by an elongation of the cotyledonary sheath or the elongated petiole (hyperphyll). For the three palm genera native to the pine rockland (Sabal, Serenoa, and Coccothrinax), Henderson (2006) classified the hyperphylls as moderate or elongate in length. The seedling of Serenoa repens (Bartram) Small was illustrated by Fisher and Tomlinson (1973), and its seedling apex was pushed about 30 mm below the seed, which was planted on the soil surface. Seedlings of Sabal palmetto (Walter) Lodd. ex Schult. & Schult. f. and Coccothrinax argentata (Jacq.) Bailey displayed the same behavior when germinated in pots in the greenhouse (J. Fisher, unpublished observations). In these palms, the first nodes of the seedling lacked axillary buds, unlike the dicotyledons examined here. The shoot axes of these palm seedlings grew deeper into the soil as an early stage of establishment growth that was described by Tomlinson (1990). There was no indication of root contraction in seedling burial, but rather a gravitropic growth response in the young seedling. Until the trunk axis began to elongate and grew upward, the apical bud was buried and protected from fire. In an analogous manner, the shoot apices of Leontice (Berberidaceae) and Astoma (Apiaceae) were inserted deeper into the soil by an elongation of the cotyledonary tube (Galil, 1970) and similarly in the conifer Araucaria (Burrows et al., 1992) and in Zamia pumila and cycads generally (Norstog and Nicholls, 1997). The initial displacement from the seed in Zamia was followed by a life-long contraction of the shoot/taproot axis (Stevenson, 1980).
Some plants have epigeal germination but lack hypocotyl elongation, thus keeping their cotyledons and associated buds at soil level as in Byrsonima and Jacquemontia (Fig. 3A) and Lanatana, Passiflora, Psidium, and Tetrazygia (Table 1). Others have hypogeal germination with the enclosed cotyledons remaining at soil level as in Pithecellobium (Fig. 3C) and Sophora (Fig. 3D, Table 1). Ecological reviews have emphasized the role of reprouters in allowing plants to persist after repeated shoot damage over long periods without recruitment of seedlings. Resprouting was an effective strategy for responding to disturbance (Bellingham and Sparrow, 2000; Bond and Midgley, 2001). New shoots arose from basal buds that were protected from fire damage by their basal or subterranean position (Snyder, 1986; Snyder et al., 1990). As would be expected, resprouters had greater root to shoot ratios, greater starch storage in their roots, and deeper perennating buds in the soil than did seeders (Pate et al., 1990, 1991; Bell et al., 1996; Schwilk and Ackerly, 2005). Many, if not all, of the pine rockland species examined here appeared to have these features in varying degrees.
The present findings indicate that some seedlings of the Florida pine rockland community actively repositioned lateral buds after germination. There were several mechanisms that lower the cotyledonary buds: (1) axis contraction by differential cell enlargement and collapse, (2) axis contraction by symmetrical production of G-fibers, (3) hypocotyl bending by asymmetrical production of G-fibers, and (4) remote hypogeal (= cryptogeal) germination in palms and Zamia that pushed the entire seedling deeper into the soil. The cotyledonary and adjacent buds at the base of the shoot (or the apical bud of the single-stemmed Coccothrinax and Sabal palms) will produce the new sprouts after fire.
Some noncontractile species had their lowest buds at or below ground level due to hypogeal germination (Pithecellobium, Sophora), epigeal germination in which cotyledons expand at the soil surface (Jacquemontia, Lantana, Tetrazygia), or relatively short hypocotyls (Byrsonima, Passiflora, Psidium). The remaining species can be expected to maintain their basal most buds some 10–20 mm above soil level, assuming there will be no later contraction of the shoot/root axis (Forestiera, Morinda, Senna ligustrina, Sida). The seedling with the longest hypocotyl (20 mm), and therefore most vulnerable to fire, was Rhus which also forms adventitious root buds that produce new sprouts or suckers unrelated to seedling growth.
In summary, the seedlings of some woody plants can reposition their cotyledonary nodes closer to the soil by axis contraction or bending. Anatomy suggested that two mechanisms operate: (1) the previously well-documented collapse of parenchyma cells in two species (Convolvulaceae and Zamiaceae), and (2) the newly documented production of G-fibers in six species (all Fabaceae). Contraction or bending of the hypocotyl and/or taproot moved the cotyledonary and later buds of the seedling closer to the soil surface or buried them. Bud repositioning by these mechanisms may protect the lateral buds from injury by fire or other environmental stresses and allow resprouting.
FOOTNOTES
1 Thanks to D. Walters for germinating seeds; J. Geiger for Ipomoea seeds; Jay Horn for advice on imaging; M. Litzinger for help with German translation; Barry Tomlinson, Joyce Maschinski, Cynthia Jones, and two anonymous reviewers for comments on the manuscript; and G. D. Gann, J. R. Snyder and J. O’Brien for sharing their unpublished field observations. Research was supported in part by Florida Department of Agriculture and Consumer Services, Division of Plant Industry contract 012863 to J. Maschinski. 
2 Author for correspondence (e-mail: jfisher{at}fairchildgarden.org)
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