GLANDULAR STRUCTURES OF HOLOGARPHA AND THEIR ONTOGENY
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1 Reprinted from the AMERICAN JOURNAL OF BOTANY. Vol 46, No. 4, April, 1959 Printed in I'. S. A. GLANDULAR STRUCTURES OF HOLOGARPHA AND THEIR ONTOGENY SHERWIN CARLQIIST
2 GLANDULAR STRUCTURES OF HOLOCARPHA AND THEIR ONTOGENY 1 SHERWIN CARLQUIST ABSTRACT CAKKH I-I, NIEKWIN. (Rancho Santa Ana Botanic Garden, Claremont. California.) Glandular structures of Holocarpha and their ontogeny. Amer. Jour. Bot. 46(4): Illus Two types of advanced glandular structures occur in the 4 species of the genus Holocarpha. Sessile disk-shaped glands occur at the tips of upper leaves and of involucral and receptacular bract-. Unlike all other glandular -irtictures of Madinae which have been investigated, these originate from several protodermal initials rather than a single one. These glands, however, represent modifications of a glandular trie-home. The other type of glandular structure, termed hollowi.iiked irirlinme here, occurs on the outer surface of involucral and receptacular bracts. These trichomes originate from a single cell but differ from others in the formation of a hollow stalk. I he wall of which is one cell in thickness. Mesophyll of the bract, often with an included vascular bundle, is present as an intrusion into the base of the hollow stalk. Corresponding to the advanced nature of the glandular structures, the leaves show specializations in the "innilling" of margin-. I i»r leaves have a cylindrical organization of vascular tissue, whereas basal leaves are "normal" and leave- of the main -inn are intermediate. The species of Holocarpha differ in certain details ol leaf anatomy and structure of hollow-stalked trichomes. The systematic distribution of these i- given. The essential unity of the various glandular structures of Madinae is discussed both in terms,,[ mature structure and ontogeny, and the steps in the evolution of these are suggested. THE GENUS Holocarpha (Compositae. subtribe Madinae) consists of 4 species (Munz and Keck, in pros i which are notable among the tarweeds b.r their higfi degree of specialization. This is reflected in their chromosome numbers I Johansen, I').">. }: Clausen , which do not appear to be basic within Madinae. as well as in the chromosome repatterning which has evidently been extensive in the genus I Clausen. 1951). In addition to features ol gross morphology, the glandular structures reveal greater specialization than do those of other tarweeds i Carlquist. 195<>t with the possible exception.. ' (tilycadenia (Carlquist. 1959). The glandular structures of Holocarpha can be divided into 1 group-: (1) biseriate trichomes which occur on herbage and involucral bracts (Carlquist, 1958; see herein, fig. 6, 19, 30); in some of these, the heads mav be subdivided into more numerous cells; (21 multiseriate. short trichomes occurring on coroqa-lobe tips (Carlquist, 19581: (3) sessile glands present at the tips of upper leaves and introlucral and receptacular bracts: (4) hollowstalked, multiseriate trichomes on the outer faces of involueral and receptacular bracts. The latter 2 categories form the basis for the present paper. 1 Received for publication Julv The structure of these types is unique among tarweeds. and ontogenetic studies were undertaken i<> aid in clarifying the relation between these glandular structures and their simpler counterparts in other genera of Madinae. The sessile glands of Holocarpha are intimately related to the leaves and involucral bracts on which the) are borne. Ontogenetic studies of the leaf itself are presented here on this account, together with data on mature leaf structure. The relatively advanced anatomy of the leaf (compared with other Madinae i provides pertinent comparisons in assessing evolution of anatomical characters within this subtribe. MATERIALS AND METHODS. Living material of Holocarpha heermannii and of H. virgata in various stages of development was collected in the field and portions were preserved in formalin-propionoalcohol. Samples of H. macradenia (which is probald\ now extinct: Clausen. 1951) and H. obconica were taken from herbarium specimens and expanded in 2.5 r «aqueous NaOH. Both types of material were embedded in paraffin according lo the usual techniques. The safranin-fast green staining series used for sections corresponds to Northen's modification of Foster's tannic acid-ferric chloride method (Johansen The pectic Substances alluded
3 April, 1959] CARLQUIST GLANDULAR STRUCTURES OF HOLOCARPHA 301 Fig Ontogeny of sessile gland in Holocarpha virgata. Fig Primordia of involucral bracts; the remainder, leaf primordia. Fig. 6. Paradermal section; the remainder, sagittal sections of primordia. Fig. 1. Leaf primordium just prior to differentiation of initials. X350. Fig. 2. Initials at tip of primordium. X475. Fig. 3. Anticlinal divisions in initials. X420. Fig. 4. First periciinal division. X480- Fig. 5. Additional divisions producing a flattened configuration at tip of primordium. X580. Fig. 6. Widening of future gland. X550. Fig. 7. Stage at which cell division is nearly complete. X370. Diagrammatic representations given in fig
4 302 AMERICAN JOURNAL OF BOTANY [Vol. 46 to below were identified by means of their deep coloration with Ruthenium Red and their solubility in warm 0.5', ammonium oxalate. Such pectic compounds, however, also exhibited a tendency to dissolve somewhat in the formalin solution used in mounting the sections on slides. Pectic accumulations appeared to be retained in NaOH-treated material to an appreciable extent. Specimens which document preserved material, or dried specimens from which material was taken, are as follows: H. heermannii. Carlquist 416 (RSA); H. rnacradenia, McMurphv X (RSA) ; H. macradeniu. Jones VI (POM), basal leaves onl\ : H. obconica, Keck and Stockwell 2501 i RSA. isotype); //. virgata, Carlquist 412 I RSA). In addition, all the herbarium specimens of Holocarpha in the Rancho Santa Ana Botanic Garden (RSA) and Pomona College (POM) herbaria were examined for data on trichome distribution. The writer wishes to thank the curators of the herbaria indicated above for the use of their materials. Appreciation is expressed to Dr. David D. Keck for bis interest in these studies. SESSILE GLANDS. The tips of upper leaves (chiefly those on abbreviated branches which terminate in heads) and of involucral and receptacular bracts bear a glandular disk (fig. 14, 15). Because the nia!lire structure of these differs so sharply from that of a trichome. the less precise term "sessile gland"* is used here. The ontogeny of these is shown in the photographs, fig. 1-7: most of these are interpreted by line drawings in fig The first perceptible stage in the development of sessile glands is the enlargement of a group of protodermal cells at the tip of a primordium I fig. 2. 9). Prior to this enlargement, all the protodermal cells are alike in size and staining properties (fig. 1, 8). There is no visible evidence that only a single cell is involved, although all the initials could conceivably have been derived ultimately from a single protodermal cell earlier in the development of the primordium. Differentiation of initials takes place on very young primordia. Anticlinal divisions in those cells destined to give rise to the gland (fig. 3, 10) widen the area of initials. This stage is followed by the appearance of periclinal divisions I fig, 4, 11) which increase the number of cell layers. Because the walls which separate protoderm from ground meristem stain more deeply, the derivation of the gland from protoderm exclusively can be demonstrated in young primordia. Cell enlargement and both anticlinal and periclinal divisions occur in such a manner that a blunt shape is imparted to the tip of the primordium (fig. 5, 12). Further periclinal divisions (fig. 6) increase the number of cell layers. Approximately three or four layers (fig. 7, 13) are set up in this manner. Further stages in the development of the gland are marked by anticlinal divisions in these layers. The future gland is widened I fig. 7, 131, and is in fact invariably wider at this stage than the primordium which bears it. At this point (fig. 7) procambium is present in the leaf primordium. Such a stage is seen in transection in fig. 17. Relatively little change in cellular constitution can be noted between a gland such as that shown in fig. 7 and the mature structure in fig. 14, 15. Cells of the gland now become filled with a resin-like substance and commence their secretory activities. Meanwhile, the vascular tissues of the leaf attain their characteristic mature configurations. Although vascular tissue of the midvein and its branches terminates near the base of the gland ' fig I. such vascular tissue does not enter it. Prominent cell elongation and Fig Diagrammatic drawings of the sagittal sections of primordia illustrated in fig. 1-5, 7. Fig. 8 = fig. 1. X350. Fig. 9 - fig. 2. X330. Fig. 10 = fig. 3. X330. Fig. 11 = fig. 4. X370. Fig. 12 = fig. 5. X380. Fig. 13 = fig. 7. X225. Heavy line separates the protoderm and its derivatives from ground meristem. Broken lines represent probable recent divisions. Fig Holocarpha virgata. Fig Longitudinal sections of tip of upper leaf, showing sessile gland. Fig. 14. Paradermal section. X240. Fig. 15. Sagittal section (adaxial side below). X270. Fig Transections of primordia of upper leaves, taken approximately midway along primordia which are.09,.14, and.72 mm. long, respectively. X350. Fig. 19. Transection of upper leaf, taken about midway along length of the leaf. X195.
5 April, 1959] CARLQIIIST GLANDULAR STRUCTURES OF HOLOCARPHA 303
6 304 AMKRICAN JOURNAL OF BOTANY [Vol. 46 enlargement occur in palisade and spongy tissues of the mesophyll, so that the leaf becomes wider than the gland. Because several protodermal initials are involved in the formation of the gland, rather than a single initial, the gland is not trichome-like in its ontogeny. Even the massive tack-shaped glands on upper leaves of Calycadenia originate from a single cell (Carlquist, 1959). In these tack-shaped glands, however, the single cell often divides into four cells which, in their subsequent division products, are not trichome-like, but reminiscent of those of sessile glands of Holocarpha. The fact that only protodermal initials are involved in the formation of the sessile glands of Holocarpha does suggest that these glands represent derivatives of trichornes. phylogenetically. Because all other glandular structures in Madinae are apparently of trichome origin, the sessile glands of Holocarpha could hardly have been derived from any other structure. Their restriction to the tips (or teeth I of leaves is like the restriction of tack-shaped glands to tips of leaves in some species of Calycadenia (Carlquist. 1959). If the sessile glands of Holocarp/ui are oi trichome origin, however, their ontogeny has been highly altered. One can formulate a series within Madinae of progressively more advanced structures. In such a series, the biseriate stage is pushed further back into ontogeny. Biseriate trichornes retain this character throughout their development. Capitate trichornes with biseriate stalks show the biseriate condition until subdivisions in the terminal portion alter this. The tack-shaped trichornes of Hlepharizonia (Carlquist. 1958) are biseriate only until four tiers of cells are formed, at which time a series of anticlinal divisions initiates a quadriseriate condition. A similar situation obtains in the smaller tack-shaped glands of Calycadenia i Carlquist, 1959). In the larger terminal glands of that genus, however, the biseriate staae consists only of a pair of cells which subdivide directly to a quadriseriate condition. Therefore, the lack of a biseriate stage in the highly advanced sessile glands of Holocarpha is not surprising. Concomitant with the progressively greater alterations in trichome-like ontogeny. there is a tendency for glandular trichornes, or glands, to be initiated earlier in ontogeny (i.e., on progressively smaller primordial. LEAF ANATOMY. As in other genera of tarweeds, leaves of Holocarpha are polymorphic within a single plant. The upper leaves seem to represent modifications, in certain respects, of the structure found in lower leaves. The peculiarities in structure of upper leaves are illustrated in fig As fig show, a central strand of procambium becomes evident at an early stage. This strand of procambium is destined to become the midvein. Procambium for all other veins originates as branches of this single strand. A stage in such branching is shown in fig. 18. Differentiation of the ground meristem of the primordium into a hypodermal layer, which subdivides into the 2 layers of palisade which surround the leaf, and the future spongy parenchyma cells, also is shown in fig. 18. The mature leaf (fig. 19: see also. fig. I1-15 I is cylindrical hi construction. The midvein (visible also in longitudinal section, fig. 15) lies beneath a layer of palisade parenchyma on the adaxial surface. The other veins form a network which encircles the leaf, so that a cylindrical con- -tiuction is evident. In the basal portion of the leaf (fig. 201, the bundles lie in a single plane. At the leaf base, all the lateral bundles join the midvein, and a unilacunar node is present. The transition between the single plane of bundles at the base of the leaf and the cylinder of veins above the base involves a curving of lateral bundles around toward the lower surface of the leaf, so that they meet along most of the length of the leaf and form a cylindrical conformation. Additional features of histologv in upper leaves of Holocarpha merit mention. The outer walls of epidermal cells are extremel] thick-walled. Apparently no cuticle is present on mature leaves. No demarcation of cuticle from cell wall can be observed, and the lack of staining by safranin suggests absence of cutin. Internal walls of the epidermis are also rather thick. Cells of the bundle sheaths are often lightly scarified, and a few fibers may be present near the phloem pole of the midvein. No bundle-sheath extensions are present. Of considerable interest is the spongv mesophyll in the center of the leaf. In the intercellular spaces between these cells, pectic compounds are accumulated, partly or entirely fillin- these spaces. Thus the center of the leaf is converted into a pectic channel, much like those described by the writer for other members of Madinae. Argyroxiphium (Carlquist. 1957) and Calycadenia (Carlquist. 1959). Leaves of the main stem of Holocarpha virgata (fig. 21 l show less specialization in vascular structure. They do show an incurving of bundles at the margins. This fact is reflected in the gross morphology of the leaf, for the "true" margin is recurved toward the lower surface. This incurving of the margins and marginal bundles is not complete, so that a cylindrical structure is not attained. The midvein is jacketed by a sclerified bundle sheath which is contiguous to fibers at the phloem pole of the bundle. A sheath extension, consisting of thin-walled parenchyma, is present. Because the sheath extension separates the two areas of spongy parenchyma and their intercellular pectic contents, two pectic channels may be said to be present. Some leaves of the main stem may be thinner than the one figured. In this case, some lateral bundles are in contact with both upper and lower palisade. Thus, more than 2 pectic channels may be present.
7 April. 1959] CARLQUIST GLANDULAR STRUCTURES OF HOLOCARPHA 305 Leaves of the basal rosette of H. virgata show a "normal" vascular structure in that the bundles lie in a single plane and no incurving of the margin is present. This condition is shown here for H. macradenia (fig. 22). Such leaves are isolateral in respect to palisade parenchyma distribution. Unlike upper leaves, they are associated with trilacunar nodes. A prominent marginal strand of fibers is present interior to the marginal vein; this feature is characteristic of many other tarweeds, such as Calycadenia (Carlquist, 1959). Bundle-sheath extensions and fibers adjacent to phloem may be present on some of the lateral veins of basal leaves. In gross morphology, leaves of the basal rosette differ from upper leaves in that teeth are present along the margins of basal leaves. The variation of structure from leaves of the basal rosette to those of the main stem and those on upper, lateral branches may be found in all species of Holocarpha. In H. macradenia. however, this transition is incomplete, because a cylindrical construction is not attained by upper leaves. Upper leaves of H. macradenia correspond to the main stem leaves of H. virgata illustrated in fig. 21. Thus the leaf morphology of H. macradenia illustrates a retention of a more juvenile form, or a less evolved condition, than the other three species. All species of Holocarpha agree in possessing persistent capitate liichomes with biseriate stalks. These occur on basal and upper leaves (fig. 19). On basal leaves, these trichomes tend to have longer stalks, resembling those figured for Madia saliva (Carlquist, 1958). The teeth of a few basal leaves may be converted into sessile glands. This was observed in some specimens of H. macradenia, H. obconica. and H. virgata. Leaves possessing such glandular teeth are not present on every plant of these species, however. The species of Holocarpha all possess uniseriate non-glandular trichomes in addition to the glandular ones. These trichomes may be long and several cells in length, and were observed on all leaves and on the stem of all specimens examined of H. macradenia and on some of H. heermannii. There appears to be a tendency toward glabrescence. however, because upper leaves of some specimens of H. heermannii and nearly all specimens of H. obconica and H. virgata show very short uniseriate non-glandular trichomes or none at all. No secretory canals were observed in any leaves of the species of Holocarpha. HOLLOW-STALKED TRICHOMES OF THE INVOLUCRE. In addition to sessile glands, the species of Holocarpha possess a type of glandular trichome which does not occur in any other tarweed. These are borne on the outer surface of involucral and receptacular bracts. They are distinctive in possessing a massive glandular head and a hollow cylindrical stalk, the walls of which are a single cell in thickness (fig. 23, 24, 31). The ontogeny of these trieliomes illustrates that, unlike sessile glands, the development suggests that of other trichomes of Madinae. Hollow-stalked trichomes originate from a single cell (fig. 25. right). An anticlinal division in a plane parallel to the long axis of the primordium initiates a biseriate condition (fig. 26; fig. 32). Periclinal divisions then produce several tier- <>\ cells in this biseriate structure, so that at this stage it corresponds to the simple biseriate trichomes of other Madinae. Anticlinal divisions then convert the biseriate structure to a quadriseriate condition. These divisions begin at the base of the trichome (fig. 25, left; fig ) and then extend to the terminal tiers (fig. 27, right; fig. 37). At this stage, the trichome is not unlike the quadriseriate stage in the development of tack-shaped trichomes of Blepharizonia (Carlquist, 1958). Subsequent steps in development of the hollow-stalked trichomes are unique, however. In the future stalk portion, anticlinal divisions form radially to the center of the four series of cells. Because of this radial orientation of all divisions in the future stalk, followed by formation of a space in its center, the wall of the stalk is only a single layer of cells in thickness (fig. 35; fig. 36, mature). This space results from separation of cells along their inner faces. Divisions in the future head of the trichome are not radial to the center of the trichome I tig. 38), but blocks of cells are set off so that by subdivision in various planes a massive multicellular structure is initiated I fig. 39). No intercellular space develops among these cells. A young trichome in which the stalk has begun to develop its hollow center is shown in fig. 28. Divisions in the head portion of this trichome are not yet complete. Such divisions begin in the subterminal lasers. and the terminal layer is subdivided last. Three cell tiers are participating in the formation of the head of the trichome seen in fig. 28. A longitudinal section of a trichome. cut at right angles to that shown in fig. 28, is illustrated in fig. 29. This trichome represents a later stage in which the hollow nature of the stalk is clearly visible. The terminal portion of the trichome has been widened by means of numerous anticlinal divisions. The trichome in fig. 30 (cut in the same plane as that of ficr. 28) illustrates approximately this same stage. Further development of the trichome is characterized by elongation of cells of the stalk. A significant feature which accompanies this, however, is the intrusion of ground meristem cells of the bract into the hollow stalk. The beginning of such intrusion is visible in fig. 30. The extent of this intrusion in mature hollow-stalked trichomes of H. virgata may be seen in fig. 31. Of particular interest is the fact that in such intrusive ground meristem of many trichomes, procambium is formed. Maturation of intrusive tissues results in the formation of a vascular bundle surrounded by palisade parenchyma. In the trichome shown in fig.
8 306 VMKRICA.N.IOI HNAL OF BOTANY [Vol. 46 Fig Fig. 20. Holocarpha virgata. Transection of basal portion of upper leaf. X135. Fig. 21. H. virgata. Transection of leaf of main stem, cut midway along length of leaf. X130. Fig. 22. H. macradenia. Transection of leaf of basal rosette, taken midway along length of leaf. X180. Fig. 23. H. macradenia. Hollow-stalked trichome from sagittal section of involurral bract. X180. Fig. 24. H. heermannii. Hollow-stalked trichome from sagiltal section of inwolucral bract. X215.
9 April, 1959] CARLQUIST GLANDULAR STRUCTURES OF HOLOCARPHA 307 Fig Stages in development of hollow-stalked trichomes on involucral bracts of Holocarpha virgata. Fig From oblique longitudinal sections. Fig , From sagittal sections. Fig. 29 from transection. Fig From paradermal sections above the surface of bract. Fig. 25. One-cell stage. X715. Fig. 26. Two-cell stage. X790. Fig. 27. Quadriseriate stages. X715. Fig. 28. Opening of stalk. X600. Fig. 29. Widening of head region. X610. Fig. 30. Immature trichome, showing elongation of stalk and intrusion of mesophyll into stalk base. X285. Fig. 31. Mature trichome. X150. Fig Stages in development of stalk, a- «m in transection of trichome. Fig Stages in development of head, as seen in transection of trichome. Fig , X485; fig. 36, X200; fig. 37, 39, X430; fig. 38, X550.
10 :;<>:; AMERICAN JOURNAL OF BOTANY [Vol , the vascular bundle (not clearly distinct from palisade cells) runs nearly to the end of the intruded tissue. The intrusive mesophyll and its vascularization may be clearly seen in the trichome of H. macradenia shown in fig. 23. This vascular tissue represents a branch from one of the veins of the involucral bract. In the mature trichome, secretory activity is indicated by the resin-like contents of the cells of the head portion. In the fresh condition, a droplet of this resin-like substance covers the head, just as a droplet covers the disk of sessile glands. Because of the massive group of secreting cells, there is a certain similarity in anatomical appearance between sessile glands and the terminal portion of hollow-stalked trichomes. One might liken the formation of a sessile gland to the development of a hollow-stalked trichome without the stalk. The absence of secretory canals in leaves and bracts of Holocarpha, as opposed to those of other tarweeds. in which canals are present, might be correlated with the variety and abundance of surface structures which apparently secrete the same type of resin-like substances as do the canals. Although all the species of Holocarpha are alike in respect to their sessile glands, there are differences among the species in respect to the hollow-stalked trichomes. The type illustrated for H. virgata also occurs in H. obconica. In H. heermannii, however, the hollow-stalked trichomes are smaller and more numerous on each bract. The smaller size is evident in the section shown in fig. 24. The stalk portion of the trichome is shorter than in H. virgata. Also, there is less intrusion of mesophyll into the stalk, and vascular tissue is less frequently present. As the specific name MIL; gests, the largest hollow-stalked trichomes in tli«- genus occur in H. macradenia (fig. 23). In cellular constitution they are not markedly different from those of H. virgata. but they are longer and wider. Intrusive mesophyll in the base of the trichome is generally more abundant, and the presence of a vascular bundle within the intrusive mesophyll is usually more frequent and more conspicuous than in H. virgata. DISCUSSION. This and the preceding papers in this series (Carlquist, 1958, 1959) have attempted to show that the glandular structures of the tarweeds are exceptionally varied in form, size, and structure. Just as patterns of evolution in the tarweeds provide interesting problems which have been studied from genetic, taxonomic. and physiologic standpoints by Clausen, Keck, and Hiesey (e.g., Clausen, 1951), the glandular structures of Madinae offer exceptional material for the study of evolution in anatomical characteristics. Investigation of ontogeny of these glandular structures is requisite for such a study, because alterations in the mature structure are best traced from their point of origin in ontogeny. The simple biseriate glandular trichome, which probably occurs in the majority of genera of Compositae, is represented throughout Madinae. From this trichome. the capitate trichome has evolved bv means of additional divisions relatively late in the ontogeny of the terminal portion of the trichome. From such capitate trichomes. the more specialized tack-shaped trichomes of Hemizonia fttchii, Blepharizonia. and Holozonia have been developed. The most complicated products of such evolution are found in the genus Calycadenia. which bears peculiar tack-shaped glands in the stalks of which vascular tissue is often present. Equallv advanced in their own wavs are the two tvpes of glandular structures of Holocarpha described above. Increasomplexity of glandular structures is accompanied by progressively earlier initiation (i.e., initials of more complicated types appear on smaller primordia). In Calycadenia and Holocarpha, the ontogeny of these glandular structures is intimately related to that of the leaf or bract itself, and tissue svstems other than the epidermal become involved in mature glandular structures. Complexity of glandular structures is parallelled bv the specializations in the structure of the leaves which bear them. CLAREMONT GRADUATE SCHOOL RANCHO SANTA ANA BOTANIC GARDEN CLAREMONT. CALIFORNIA LITERATURE CITED Cuu.onisT, S Leaf anatomy and ontogeny in Argyroxiphium and Wilkesia (Compositae). Amer. Jour. Bot. 44: Structure and ontogeny of glandular trichomes of Madinae. Amer. Jour. Bot. 45: The leaf of Calycadenia and its glandular appendages. Amer. Jour. Bot. 46: 7(V80. CLAI BEN, J Stages in the evolution of plant species. Cornell Univer-ity Pros. Ithaca. JOHANSEN, D. A Cytology of the tribe Madinae, family Compositae. Bot. Gaz. 95: Plant microtechnique. McGraw-Hill Book Co. New York. MUNZ. P. A., AND D. D. KECK. A California flora. University of California Press. Berkeley (in press).
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