Colleter morphology in Pavetta, Neorosea and Tricalysia (Rubiaceae) and its relationship to the bacterial leaf nodule symbiosis

Buds removed from herbarium specimens were processed for light microscopic examination of colleter form and anatomy. Most Pavetta species have dendroid colleters and bacterial leaf nodules, a correlation also found in an earlier study of Psychotria. Colleters of Neorosea , another genus with leaf-nodulated species, are more like the standard rubiaceous type that predominates in the family except that they have irregular, bulging epidermal cells. Tricalysia , a nodule-free genus closely related to Neorosea , shows a range of colleter form from standard to dendroid, and some species have the Neorosea type of colleter. Such morphological correlation between the bacterial leaf nodule symbiosis in Pavetta and Psychotria and dendroid colleters may indicate a chemical change in colleter secretion. Apart from their involvement with the bacterial symbiosis, rubiaceous colleters have now been shown to vary sufficiently in certain taxa to be considered as additional useful taxonomic characters.     

Comparative systematic study of colleters and stipules of Rhizophoraceae with implications for adaptation to challenging environments

Colleters are multicellular secretory structures found on various organs in flowering plants. Colleters on the adaxial sides of stipules have been hypothesized to play a role in protecting the developing shoot. Rhizophoraceae is a stipulate family with a broad distribution from mangrove to montane environments, which makes the family well suited for the examination of this hypothesis, but the colleters of Rhizophoraceae are not well known. We compared species from all three tribes of Rhizophoraceae, including five inland genera and all four mangrove genera. In all species, several to hundreds of colleters, sessile or stalked, arranged in rows aggregated in genus‐specific shapes, are found at the adaxial bases of open and closed stipules. Pellacalyx uniquely has additional colleters at the stipule margins. Colleters are all of the standard type, comprising a central axis of core parenchyma with large vacuoles and tannins, and an outer palisade‐like epidermis with organelles involved in secretory activity. An exception is Pellacalyx axillaris, in which colleters appear as extremely small epidermal protrusions. Kandelia obovata has a tracheary element in some colleters. Pellacalyx uniquely has an unusual fleshy outgrowth on the adaxial stipule base. We propose an evolutionary sequence in which Macarisia has plesiomorphic stipule and colleter traits and the mangrove Kandelia obovata with colleter vascular traces is most derived. Colleter and stipule structures are largely concordant with habitat and phylogeny, and show taxonomic value. The strong alignment of colleter and stipule patterns with habitat is suggestive that colleters have a protective function, although some components of these patterns may be phylogenetically determined. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 172 , 449–464.     

MORPHOLOGY AND DISTRIBUTION OF COLLETERS AND CRYSTALS IN RELATION TO THE TAXONOMY AND BACTERIAL LEAF NODULE SYMBIOSIS OF PSYCHOTRIA (RUBIACEAE)

Earlier investigators established that a finger-like colleter with elongate axial cells and a palisade epidermis is the standard type in the Rubiaceae. This type, with some variation, also prevails in Psychotria, based on a worldwide anatomical survey of vegetative buds from herbarium specimens of 296 species (about 50 % of total). It is virtually the only type found outside of continental Africa. Among African species, it is most common in subgenus Psychotria, with mostly nodule-free species. In subgenus Tetramerae, with only leaf-nodulated species, there is a strong tendency toward brushlike and dendroid colleters in which epidermal cells are extremely elongate and separated from each other. It is speculated that this change in colleter morphology associated with presence of nodule bacteria may be correlated with a change in secretion product more suitable for support of bacteria. Three morphological forms of crystal occur: raphides, styloids, clustered crystals. They may occur singly or in combination. Several patterns and trends were noted in crystal distribution that could be of taxonomic significance.     

Structural, Functional and Phylogenetic Aspects of the Colleter

This article surveys the structural, functional and phylogeneticsignificance of colleters in different dicotyledonous families.Colleters are multicellular secretory structures attached tothe stipule, petiole, lamina, bract, bracteole, calyx and corolla.Colleters are grouped into standard (S), dendroid (D) and brush-like(B) types on the basis of their morphology and structure. Dand B-type colleters occur in certain members of Rubiaceae thatalso have bacterial leaf nodules. Besides the normal structure,epithelial hairs, thin-walled subepidermal cells, laticifersand vasculature are present in many colleters of Apocynaceae.It is probable that the colleter functions to protect the developingmeristem by secreting a viscous fluid. Exudate of D-type colletersare mucilaginous, providing the substrate necessary for thenutrition of endophytic bacteria. Colleter, structure, phylogeny     

Anatomical structure and secretion compounds of colleters in nine Ilex species (Aquifoliaceae) from southern South America

In order to clarify whether the structures observed at the base of the petiole of the genus Ilex are colleters resulting from stipules, the anatomy, vascularization and secretions of these supposed glandular structures were analysed in nine species. This is the first report of colleters in Ilex. Stipular colleters replace the stipules in all species studied and are characterized by the presence of vascular traces. In addition to the stipular colleters, three other types of colleter were distinguished: standard and lachrymiform colleters found on the leaf teeth or crenations, and sessile colleters found on the margins of the floral bracts. Their basic structure consists of a central core of parenchymatous cells surrounded by one layer of palisade secretory epidermal cells. Histochemical tests were also performed on secretions; proteins were found in the secretions studied, but glucose was not. The glandular origin of the stipular colleters is confirmed on the basis of their position, secretions and anatomy. Analyses of the colleter‐secreted proteins distinguished two different groups of Ilex species. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 160 , 197–210.     

Histochemistry and Senescence of Colleters of Allamanda cathartica (Apocynaceae)

Allamanda have colleters on the adaxial bases of petiole, bractsand bracteoles. Each colleter is finger shaped, differentiatedinto a long head on a short stalk. Vasculature to the colleteris absent but branched laticifers are present among the centralcells. Secretion of the colleter contains glucose and rhamnose.The major elements present in the exudate are Na, Fe and Zn.Starch, protein and lipids were identified, with lipids themajor component. Petiolar colleters are persistent and becomestiff due to the lignification occurring in the walls of epithelialand central cells. Because of over-lignification in the centralcells, the cell lumen is highly reduced. Allamanda, colleter, laticifer, secretion, senescence     

Trichome forms in Ardisia (Myrsinaceae) in relation to the bacterial leaf nodule symbiosis

Symbiotic leaf-nodule bacteria in nodulated members of Rubiaceae live in mucilage secreted by colleters located on stipules within buds. These differ from colleters on most nodule-free species. This study was undertaken to examine buds of Ardisia and the related monotypic Amblyanthus of Myrsinaceae to see if nodulated species had secretory structures dissimilar from those of nodule-free species. Buds removed from herbarium specimens (61 species) and live plants (3 species) were paraffin-sectioned. Diverse trichome forms occur, including dimorphism between adaxial and abaxial trichomes in some species. Species within each subgenus were arranged according to trichome form: peltate scale, irregularly capitate, capitate, sessile capitate, bicellular capitate, and uniseriate. Only seven Ardisia species (all in subgenus Crispardisia, widely assumed to have bacteria in marginal leaf nodules of all 30 species) have short-lived trichomes bearing one or more elongate, swollen, distal cells that appear to be secretory cells. These trichomes are analogous to the dendroid or brushlike colleters of nodulated Rubiaceae. Druses occur in most subgenera and this appears to be by far the most predominant crystal type m Ardisia.     

Anatomy and histochemistry of colleters in Roupelia grata (Apocynaceae)

The colleters of Roupelia grata are present on the petiole of the leaf, bract, bracteole and calyx. A mature colleter has a distinct head and a stalk. The parenchymatous central core is surrounded by epithelial cells. The senescence of the colleter occurs at its apex first and then proceeds towards the base.     

Leaf colleters in Tontelea micrantha (Celastraceae,Salacioideae): Ecological,morphological and structural aspects

The colleter secretion can be useful to protect plants of Cerrado (Brazilian savanna) biome during the long and pronounced dry season. This study describes the presence of colleters in Tontelea micrantha and represents the first record of these structures in Celastraceae. To investigate colleter structure and their secretory processes, young leaves were collected, fixed, and processed according to conventional techniques for light, and electron microscopy. Colleters were observed at the marginal teeth on the leaf. They produce mucilaginous secretions that spread over the leaf surface. After secretory phase, colleters abscise. The secretory epithelium is uniseriate and composed of elongated cells whose dense cytoplasm is rich in organelles. The ultrastructure of the secretory cells is compatible with the pectin-rich secretion. Observations of the young leaves surface revealed the presence of superficial hydrophilic secretion films that appeared to have the function of maintaining the water status of those organs.     

Calycine colleters of seven species of Apocynaceae (Apocynoideae) from Brazil

The structure and organization of calycine colleters belonging to four genera of Apocynaceae are described. Calycine colleters were found in all species. All colleters had the same histological composition, but morphological differences were observed in four species. Most colleters were of the standard type, and possible deviations resulted in three morphological types: bifurcated, laminar, and sessile. Mechanisms of cell separation, proliferation, and elongation may explain the origin of the new types. As a consequence of morphological changes, the secretory surface was expanded in the bifurcated, laminar, and sessile glands. Most colleters were in a post-secretory phase, but a hydrophilic secretion was observed in Mandevilla pycnantha and Mesechites mansoana . A larger secretory surface, together with the extension of the secretory phase in adult flowers, were major shifts in the calycine colleters of Apocynaceae, and are possibly correlated with the functional and ecological aspects of these organs. Three patterns of distribution of calycine colleters were observed: alternate, opposite, or indefinitely distributed. The alternate pattern was not homogeneous, and three subtypes were recognized: four-, five-, and ten-grouped colleters. The number of calycine colleters was variable between taxa and even within the same species.  © 2006 The Linnean Society of London, Botanical Journal of the Linnean Society , 2006, 152 , 387–398.     

The Development, Structure and Function of Dendroid Colleters in Psychotria kirkii Hiern (Rubiaceae)

The dendroid colleters of the leaf nodulated Rubiaceous shrubPsychotria kirkii Hiern. have been studied with respect to theirdevelopment, structure and function. The colleters, which arisefrom the adaxial surface of stipules of apical and lateral shoots,secrete a protein/carbohydrate mucilaginous substance in whichis maintained a colony of leaf nodule bacteria. The colletersare multicellular and multiseriate, consisting of a two to fourcell thick stalk from which radiate up to 70 elongate secretorybranch cells. Cuticle envelops both stalk and branch cells inearly developmental stages and as secretory activity increasesthis cuticle is largely lost in two different ways. The majorpart is forced off the branch cell surface through the passageof a largely carbohydrate component of the mucilage which surroundsthe colleters: a second method of cuticle loss involves thepassage from the cell of small electron-translucent bodies whichbecome coated with cuticle as they exit the cell. The mucilagein which the bacterial cells are found provides a vehicle wherebythe bacteria are able to enter the leaves, thus leading to theinitiation of leaf nodules. Psychotria kirkii Hiern., secretory dendroid colleters, symbiosis, ultrastructure, trichome development     

Ontogenesis, structure and ultrastructure of Hymenaea stigonocarpa (Fabaceae: Caesalpinioideae) colleters

The genus Hymenaea is characterized by a great diversity of secretory structures, but there are no reports of colleters yet. The objectives of this study are to report the occurrence and describe the origin and structure of colleters in Hymenaea stigonocarpa Mart. ex Hayne. Shoot apex samples were collected, fixed, and processed for light microscopy, scanning electron microscopy, and transmission electron microscopy as per usual methods. Colleters occur predominantly on the stipule's adaxial side. These structures are found at the base on a narrow strip, corresponding to the median vein up to half the length of the stipule. When present on the abaxial side, they are concentrated at the base and restricted to the margins. Colleters develop from the protoderm; they are elongate and club-shaped. Their body has no stratification; their surface cells differ from the inner cells only in position and presence of cuticle. Colleter cells have thin walls, dense cytoplasm, large nuclei, many mitochondria, rough endoplasmic reticulum, and abundant dictyosomes. Histochemical tests with Ruthenium red showed pectic compounds in the cytosol. In H. stigonocarpa, colleter arrangement is compatible with the hypothesis that they protect shoot apex. In this species, protection is reinforced by the sheath formed by the stipule pairs.     

Dendroid colleters on vegetative and reproductive apices in Alibertia sessilis (Rubiaceae) differ in ultrastructure and secretion

In this work we compare the structure and secretion of dendroid colleters on stipules, bracts and sepals of Alibertia sessilis, a non-nodulate Rubiaceae species from Brazilian cerrado, with notes on the plant phenology. Samples were processed according to usual methods for anatomy, histochemistry and ultrastructure. Colleters are conical and constituted by a central axis of elongated parenchyma cells from which radiate numerous epidermal cells. Epidermal cells are cylindrical on the vegetative apex and digitiform or bulbous on reproductive apex. Both colleters produce hydrophilic and lipophilic compounds. On the vegetative apex, epidermal cells present numerous well-developed Golgi bodies associated with a network of smooth endoplasmatic reticulum (SER), scarce oil bodies and profiles of rough endoplasmatic reticulum (RER), indicating the involvement of these glands in the production of mainly polysaccharides in addition to protein and lipids. Differently, epidermal cells on bracts and sepals present abundant and prominent oil drops, fewer Golgi bodies and a well developed network of SER with locally dilated cisterns indicating predominance of lipids. Ecrine and granulocrine mechanisms are common to colleters of both apices. We hypothesize that exudates protect vegetative meristems and developing organs against desiccation in the dry season and against insects and pathogens during the wet season. Predominantly lipidic secretion protects the floral organs against dehydration in the dry season and can attract floral visitants. These aspects are relevant if one considers that A. sessilis inhabits the cerrado, an environment characterized by a well-delimited dry season, high irradiance and elevated vapor pressure deficits.     

The structure of colleters in several species of Simira (Rubiaceae)

BACKGROUND AND AIMS: Colleters are secretory structures consisting of a parenchymatic middle axis surrounded by a layer of palisade-like epidermal cells. Colleters occur in a large number of rubiaceous species. Their function is to protect the developing shoot apex. They are also taxonomically useful in the Rubiaceae. This study characterized the structure of the colleters of Simira glaziovii, S. pikia and S. rubra and the biochemistry of secretions in S. glaziovii. METHODS: Stipules of the shoot apices of the three species studied were collected at Barragem de Saracuruna, in Rio de Janeiro state, Brazil. The samples were fixed according to the usual methods for light and electron microscopy. Secretion stipules of S. glaziovii were washed with 0.1 m Tris-HCl plus 0.1 %Triton X-100 to extract proteins and carbohydrates. KEY RESULTS: Colleters in these species are located at the base of the stipule. Each species shows a different pattern of distribution. They form as emergentia from the stipules. Simira glaziovii was different from the other two species because it exhibited vascular traces. The epidermal cells of colleters have dense cytoplasm, nuclei, small vacuoles, endoplasmic reticulum, Golgi apparatus, mitochondria and extraplasmic spaces if they are secretory. The outer cell wall of the mature colleters differs from the outer cell wall of stipule cells and immature colleters. Both carbohydrates and proteins were found in secretions from the stipules of S. glaziovii. CONCLUSIONS: Few ultrastructural differences were noted among the three species. These secretory structures not only protect the shoot apex, but also have taxonomic importance below the genus level.     

Development, Structure and Cytochemistry of Resin-secreting Colleters of Gardenia gummifera (Rubiaceae)

The structure, ontogeny and cytochemistry of stipular colletersof Gardenia gummifera are described. The repeated division ofa few adaxial protodermal and subprotodermal cells of the youngstipule and the subsequent elongation by the latter resultsin the formation of a standard-type colleter. A developed colleterhas outer palisade-like glandular cells covered by a continuouscuticle and inner layers of elongated columnar cells. Enzymelevels in the palisade-like epidermal cells in the colletersindicate their active role in secretion. The secretion is resinous,occurs in the young colleters, and accumulates between the cellsand the cuticle. The cuticle later ruptures and releases thesecretory product, which drenches the young shoot apex. Gardenia gummifera L, stipule, colleters, resin, ontogeny, cytochemistry     

Colleters in Turnera and Piriqueta (Turneraceae)

The anatomy of colleters was examined by light and scanning electron microscopy in 25 species of Turnera and nine species of Piriqueta. Based on morphology, four categories of colleters were recognized: standard, sessile, lachrymiform and trochleariform, all of which differ in shape and length/width ratio. They all have a similar anatomy: they consist of an axis of parenchymatous cells, sheathed by a palisade epidermis. The standard type is the most widespread in the studied taxa; the lachrymiform example was found in those species of Piriqueta with setiform glandular hairs; only one trochleariform example appeared in T: diffusa. The sessile type is considered to be a morphological transitional form between extrafloral nectaries and colleters. This is the first record of sessile, lachrymiform and trochleariform colleters. The anatomy of colleters is compared with other secretory structures such as glandular trichomes and extrafloral nectaries.     

Secretory hairs in Gentiana and allied genera (Gentianaceae, subtribe Gentianinae) from the Iberian Peninsula

Eleven species from six different sections of the genus Gentiana , as well as one species each of genera Gentianella (G. campestris), Gentianopsis (G. ciliata), Comastoma (C. tenellum) and Swertia (S. perennis) have been studied by light microscopy for the presence of hairs in floral as well as in vegetative parts. Hairs are produced in the calyx and vegetative leaves of all of them, and also in the corollae of the last three species. They fall into two different types: those found in the corolla of Gentianopsis ciliata are non-secretory, while in the rest of the species studied, and also in the calyx and leaves of G. ciliata , they produce a mucilaginous secretion. Calycine and foliar hairs are always produced in the adaxial epidermis at the base of the foliar organ, and are considered as mucilage secreting colleters. The presence of colleters in vegetative organs has not been adequately considered in previous taxonomic accounts, in spite of their presumed significance.     

Devonian and Carboniferous dendroid graptolites from Belgium and their significance for the taxonomy of the Dendroidea

Devonian and Carboniferous dendroid graptolites from Belgium are evaluated and partly revised. New finds in two different stratigraphic intervals of the ‘Carrière de Lompret’, an active quarry exploiting Frasnian limestones and shales east of Frasnes-lez-Couvin, allow the identification of Callograptus sp. and Dictyonema fraiponti, both belonging to the dendroid family Acanthograptidae. The relatively high diversity of the dendroid graptolite fauna from the Viséan Marbre noir de Denée, one of the few Carboniferous graptolite faunas in the world, can be shown to be based on astogenetic and preservational aspects. Nearly all known specimens can be included in the highly variable Dictyonema fraiponti, a fan-shaped large dendroid species with complex stipes formed from tubular thecae, possessing simple to complex bridges connecting adjacent stipes. Some of the graptolite material is well preserved and provides important information on the tubarium construction of Devonian to Carboniferous dendroid graptolites and, thus, is highly significant for a taxonomic and phylogenetic understanding of the youngest dendroid graptolite faunas worldwide. The genera Callograptus and Ptiograptus are revised based on their type species (Callograptus elegans from Quebec, Canada; Ptiograptus percorrugatus from the Silurian or Devonian of Kentucky, USA) and referred to the Acanthograptidae.     

Leaf Nodule Development in Psychotria kirkii Hiern. (Rubiaceae)

The initiation, development and structure of the leaf nodulesof the Rubiaceous shrub Psychotria kirkii Hiern. has been studiedin detail at the ultrastructural level. Bacteria, maintainedin the shoot tip in the secretions from dendroid colleters,invade the substomatal chamber of stomatal pores which formprecociously on the abaxial leaf surface. Proliferation of theepidermis around the pore pushes the bacterial cavity deep intothe lamina, thus forming a small internal nodule. Endophyte-mediatedschizogeny of the cells surroundng the nodule causes it to expandwhile at the same time giving rise to an interconnected reticulumof invasive host cells which are involved in metabolite exchangebetween microoganisms and host plant. Bacterial morphology changesafter entry of the microsymbiont into the host plant and, bythe time the nodule is mature, the bacteria exhibit distinctpleomorphism. Senescent nodules are shown to accumulate lipidand starch. The developmental process is discussed in the lightof existing information on this symbiosis. Psychotria kirkii, leaf nodule development, symbiosis, ultrastructure     

广东古兜山自然保护区蕨类植物群落的特征

通过对广东新会古兜山自然保护区中108个5m ×5m的蕨类植物样方调查,初步分析了样方中蕨类植物的种类组成和区系特点及种群的多度、频度、重要值、蕨类的生长型、叶的性质和群落的外貌、季相等群落学特征。结果表明:(1)古兜山自然保护区的蕨类植物种类具有典型的南亚热带植物区系特点,热带亚洲植物区系成分对古兜山蕨类植物区系有强烈影响;(2)由于蕨类植物种群的随机分布和环境因子的异质性,种群的多度和重要值分布表现出明显的正态分布规律;(3)样方中蕨类植物的形态外貌、叶的性质及其群落的外貌和季相均表现出典型的南亚热带蕨类植物群落特征;古兜山自然保护区的蕨类植物可划分为花篮状蕨类、树蕨类、匍匐类、攀援类、附生类5种生长型类型。