POLLEN BRUSH OF PAPILIONOIDEAE (LEGUMINOSAE): MORPHOLOGICAL VARIATION AND SYSTEMATIC UTILITY

The pollen brush commonly is referred to as a “bearded” or “pubescent” style in taxonomic literature and traditionally is taken to be an aggregation of trichomes on the distal end of the style, and occasionally including the stigma. We present data that support the taxonomic utility of the pollen brush but define it more specifically as a dense aggregation of erect trichomes emanating from the style (not stigma or ovary) and functioning in secondary pollen presentation. We recommend avoiding such vague terminology as bearded or pubescent styles as these refer not only to the pollen brush but also to ciliate and penicillate stigmas and ciliate styles. The latter three conditions have some taxonomic use, and since their occurrence is not necessarily correlated with the presence of a pollen brush, they should be distinguished from it. We estimate that the pollen brush has arisen independently in the following eight taxa: 1) Crotalaria and Bolusia (Crotalaraieae), 2) subtribe Coluteinae (Galegeae), 3) Tephrosia subgenus Barbistyla (Millettieae), 4) Adenodolichos (Phaseoleae subtribe Cajaninae), 5) Clitoria (Phaseoleae subtribe Clitoriinae), 6) the subtribe Phaseolinae (Phaseoleae), 7) the Robinia group (Robinieae), and 8) the tribe Vicieae. Its hypothesized homology within each of these groups is supported by a cooccurrence with other taxonomic characters, both morphological and molecular.     

Sexual selection of anther trichomes and sexual dimorphism in Ibervillea lindheimeri (Cucurbitaceae: Melothrieae)

Ibervillea lindheimeri is a dioecious member of the Cucurbitaceae whose male flowers possess a number of sex-specific characteristics including eglandular trichomes on the anther connective. A 2-year study (1989 and 1990) was undertaken to assess the potential for sexual selection of anther trichome number as a male floral trait that enhances pollen removal (a male fitness component). Correlation analysis of ten reproductive and floral traits showed that only the mean number of anther trichomes per flower was significantly associated with mean pollen removal per flower. Anther trichomes are two-celled, consisting of a small, caplike, apical cell and a large, bulbous basal cell. The basal cell is under tension and produces a sticky polysaccharide that is forcefully ejected upward when the apical cell is broken off by visiting bees. The sticky polysaccharide accumulates on the bees and aids in adherence of pollen. We propose that there is directional selection on individual males for number of anther trichomes per flower. The more anther trichomes per flower, the more pollen exported, and the greater the likelihood of siring seeds. Males differed significantly in mean number of anther trichomes per flower and were relatively consistent in their rank order over a 2-year period; both are prerequisites for sexual selection to operate. Selection coefficients and differentials for 1989 and 1990 were 0.005 and 0.007, and 0.22 and 0.32, respectively, and suggest moderate to strong directional selection on anther trichome number.     

Contributions to the anatomy of Sararanga (Pandanaceae)

Preliminary study shows the two species of Sararanga to differ considerably in morphology and anatomy. The presence of stellate trichomes in S. philippinensis is a major character separating the two species; such trichomes are not found elsewhere in the family. Massive strands of thickened cells (buttresses) extend across the leaf of S. sinuosu but appear absent from S. philippinensis. The leaf anatomy of the latter more closely resembles that common in Freycinetia. The photosynthetic tissue is not clearly differentiated into distinct layers. Both species of Sararanga have unspecialized stomata. The presence of raphides in different structures in the two species may be distinctive. The pollen grains are ellipsoidal, with an intricate reticulate exine. The fruits contrast in structure with those of Pandanus and Freycinetia and the seeds of Sararanga philippinensis have a characteristic elaborate testa.     

Correlated evolution of leaf shape and trichomes in Begonia dregei (Begoniaceae)

Structural features of leaves, including size, shape, and surfaces, vary greatly throughout the plant kingdom. In both functional and phylogenetic analyses of leaves, the various morphological aspects are often considered independently of each other, although it is likely that many combinations of features do not occur at random due to either functional constraint or genetic correlation. The distribution of variation in leaf morphology in the highly variable Begonia dregei species complex was examined in natural populations and in F(2) offspring from a cross between plants from two populations. Leaf shape was quantified using several morphometric measures, and trichomes on leaves were counted and measured. Correlations between leaf shape and the numbers and size of trichomes were examined. There were significant correlations between the shapes of leaves and the presence, number, and size of trichomes among populations and in hybrid plants. Deeply incised leaves had larger numbers of longer trichomes at the sinuses. Higher numbers of trichomes on upper leaf surfaces occurred together with trichomes at the petiole and on the abaxial surface. The potential for independent evolution of leaf shape and trichomes in this group is limited. Hypotheses to explain the correlated development of leaf shape and trichomes are discussed.     

Leaf pubescence mediates the abundance of non-prey food and the density of the predatory mite Typhlodromus pyri

Plants with leaves having numerous trichomes or domatia frequently harbor greater numbers of phytoseiid mites than do plant with leaves that lack these structures. We tested the hypothesis that this pattern occurs, in part, with Typhlodromus pyri because trichomes increase the capture of pollen or fungal spores that serve as alternative food. Using a common garden orchard, we found that apple varieties with trichome-rich leaves had 2–3 times more pollen and fungal spores compared to varieties with trichome-sparse leaves. We also studied the effects of leaf trichome density and pollen augmentation on T. pyri abundance to test the hypothesis that leaf trichomes mediate pollen and fungal spore capture and retention and thereby influence phytoseiid numbers. Cattail pollen (Typha sp.) was applied weekly to mature ‘McIntosh’ and ‘Red Delicious’ trees grown in an orchard and, in a separate experiment, to potted trees of the same varieties. ‘McIntosh’ trees have leaves with many trichomes whereas leaves on the ‘Red Delicious’ trees have roughly half as many trichomes. With both field-grown and potted trees, adding cattail pollen to ‘Red Delicious’ trees increased T. pyri numbers compared to ‘Red Delicious’ trees without pollen augmentation. In contrast, cattail pollen augmentation had no effect on T. pyri populations on ‘McIntosh’ trees. Augmentation with cattail pollen most likely supplemented a lower supply of naturally available alternative food on ‘Red Delicous’ leaves and thereby enhanced predator abundance. These studies indicate that larger populations of T. pyri on pubescent plants are due, in part, to the increased capture and retention of pollen and fungal spores that serve as alternative foods. This revised version was published online in July 2006 with corrections to the Cover Date.     

Trichome micromorphology of Iranian Stachys (Lamiaceae) with emphasis on its systematic implication

Trichomes of 37 taxa of the genus Stachys and one species of Sideritis (S. montana) were examined using light and scanning electron microscopy. The indumentum shows considerable variability among different species, but is constant among different populations of one species, and therefore, affords valuable characters in delimitation of sections and species. The characters of taxonomic interest were presence of glandular and non-glandular trichomes, thickness of the cell walls, number of cells (unicellular or multi-cellular), presence of branched (dendroid) trichomes, presence of vermiform trichomes, orientation of trichomes in relation to the epidermal surface, curviness of trichomes, and presence of papillae on trichome surface. Two basic types of trichomes can be distinguished: glandular and non-glandular trichomes. The glandular trichomes can in turn be subdivided into subtypes: stalked, subsessile, or sessile. The stalks of the glandular trichomes can be uni- or multi-cellular. Simple unbranched and branched trichomes constitute two subtypes of non-glandular trichomes. Our data do not provide any support for separation of Sideritis from Stachys. The following evolutionary trends are suggested here for Stachys: vermiform trichomes with stellate base are primitive against vermiform trichomes with tuberculate base, long vermiform trichomes are primitive against the short simple trichomes, appressed trichomes are advanced against spreading ones, and loss of glandular trichomes is advanced against their presence. Overall, trichome micromorphology is more useful in separation of species within sections rather than characterizing large natural groups known as sections, except for few cases.     

Fine structural analysis of the thoracic longitudinal stripes of Zaprionus vittiger (Diptera)

The structure of the longitudinal zebra stripes on the thorax of adult Zaprionus vittiger has been investigated by light-, polarization-, transmission electron-, and scanning electron microscopy. Each stripe consists of a central white stripe of about 50 μm width and two lateral dark brown stripes about 30 μm wide. Three different types of trichomes occur: Very long bent trichomes of the grooved-type, long bent trichomes of the crested-type, and short straight trichomes. The central white stripe contains neither bristle organs nor short straight trichomes but carries many long bent trichomes most of which are of the grooved type, contain two cavities and polarize the light in the polarization microscope. The dark brown stripes carry bristle organs and many trichomes of the short and straight-type. Bent trichomes of the crested-type are found on the whole zebra stripe at about equal frequencies; they contain no cavities and do not polarize the light. The cuticle of the dark stripes is underlain by pigment cells. It is suggested that the pigment granules in the epidermal cells cause the dark color of the dark brown stripes, whereas the form and structure of the bent grooved type trichomes cause the white color of the central stripe.     

Isolation and Analysis of Differential Expressed ESTs from Stem Trichomes of Lycopersicon esculentum (Solanaceae)

Glandular trichomes are special organs involved in plant defense response and synthesis of volatile secondary metabolites, analyzing trichome specific expressed sequence tags will help us further understand the specific function of plant trichomes. In this paper, suppression subtractive hybridization（SSH） based on magnetic beads technology was used to isolate differential expressed genes of the glandular trichomes in Lycopersicon esculentum. The differential expressing cDNA library was constructed using the glandular trichomes cDNA as tester and the cDNA from the stem without glandular trichomes as driver. After randomly sequencing 108 differential ESTs, Blast2go program was used to do blastx, functional annotation and metabolism analysis. The results show that most ESTs are related to substance metabolism, response to stress, biotic or abiotic stimulus, and have binding and catalytic function. These differential genes lay the foundation for further research on defense mechanism of the tomato trichomes.     

Morphological diversity and function of the stigma in Ficus species (Moraceae)

The stigma plays several roles such as pollen hydration and selection, and pollen tube nutrition. In the Ficus-fig wasp mutualism, stigmata have an additional, almost unknown, function by representing a physical interface for both plant and wasp reproduction. We used light and electron microscopy to compare the detailed morphology of the stigmata of nine Ficus species of different sections and with different pollination modes and sexual expressions. Figs were collected at the stage when the stigmata were receptive for pollination. Stigmata in actively pollinated monoecious species have well developed papillae concentrated on the adaxial surface exposed towards the fig cavity. Conversely, the passively pollinated monoecious species have the whole surface of the stigmata covered by somewhat smaller papillae. In both actively and passively pollinated monoecious species these features are consistent, irrespective of style length. In all actively pollinated gynodioecious species, the stigmata of pistillate flowers were tubular or infundibuliform whereas in almost all actively pollinated monoecious species (except F. racemosa) the stigmata were filiform, with one branch or two asymmetric branches. In gynodioecious species the short-styled flowers in “male” figs show a limited receptive surface with small papillae, while the stigmata of long-styled flowers in “female” figs are covered by papillae that extend down the sides of the style, increasing the stigmatic surface. In actively pollinated species, stigmata are cohesive, forming a common surface for pollen tube germination (= synstigma). The synstigma arrangement was quite variable: lax, cohesive or very cohesive, with entanglement by stigmatic papillae and stylar trichomes. Entanglement by stylar trichomes is common in gynodioecious species. The synstigma arrangement did not correlate with phylogeny or breeding system. This study is the first to report a very loose synstigma in actively pollinated monoecious Ficus species. Our analyses revealed that, in Ficus, the synstigma is functionally analogous to an extra-gynoecial compitum. Comparative studies will be required to test further hypotheses about the evolutionary determinants of such variation.     

Anatomy, palynology and nutlet micromorphology of Turkish endemic Teucrium sandrasicum (Lamiaceae)

In this study, the anatomical features of the leaf and stem, besides the pollen and nutlet characteristics of Teucrium sandrasicum are investigated. T. sandrasicum, belonging to sect. Teucrium, is an endemic perennial herb growing on serpentine around Muğla province. The anatomical studies on T. sandrasicum revealed that the stem shares the general characteristics of the Labiatae family. The leaves clearly exhibit xeromorphy due to features such as the distribution of stomata on the lower surface (hipostomatic), the occurrence of guard cells below the epidermis (xeromorphic type), inrolled margins, thick cuticle layer, thick outer epidermal cell wall, a high density of trichomes and thick palisade layer of the mesophyll. The anatomical studies showed that the upper epidermal cells of the leaf include many spherocrystals. The pollen grains are prolate, medium in size, 3-colpate with verrucate ornamentation. The nutlets are ellipsoid with a reticulate-verrucate surface. The results have proven that T. sandrasicum is different from the other species of the sect. Teucrium because of the branched trichomes on the stem and the lack of eglandular trichomes on the nutlets.     

Tissue organisation,pollen receptivity and pollen tube guidance in normal and mutant stigmas of the grass Pennisetum typhoides (Burm.) Stapf et Hubb.

Summary The normal stigma of Pennisetum typhoides is twin-branched, each branch bearing unbranched trichomes. As is general among the grasses, the papillate cells of the trichomes possess a discontinuous cuticle with overlying protein and polysaccharide secretions. These adaptations for pollen capture and hydration are absent from the stigma axes. Pollen tubes emerging from grains received on the trichomes are guided into the axes with the tips directed towards the ovary by the architecture of the basal cell complex. There are no defined transmitting tracts in the stigma axes, and further passage is through intercellular spaces of a tissue of elongated cells between the epidermis and the central vascular strands. In the mutant tr, tr, the stigmas are twin-branched, but lack trichomes. However, the principal adaptations of the trichome cells for the capture and hydration of pollen are expressed in the epidermal cells of the branches, which have permeable cuticles and the characteristic surface secretions. Pollen tubes emerging from grains germinating on the branches enter between the files of epidermal cells, or at their ends. In the absence of the guidance provided by trichome structure in the normal stigma, they pass indifferently either towards or away from the ovary. The implications of the comparison between the normal and mutant genotypes for understanding the requirements for pollen capture, germination and pollen-tube guidance in the grasses are discussed.     

Herbivore handling of a Plants trichome: the case of Heliconius charithonia (L.) (Lepidoptera: Nymphalidae) and Passiflora lobata (Killip) Hutch. (Passifloraceae)

Trichomes reduce herbivore attack on plants by physically and/or chemically inhibiting movement or other activities. Despite evidence that herbivores are negatively affected by trichomes there also reports of insect counter-adaptations that circumvent the plants defense. This paper reports on a study that investigated the likely mechanisms employed by larvae of the nymphalid butterfly, Heliconius charithonia (L.), that allow it to feed on a host that is presumably protected by hooked trichomes (Passiflora lobata (Killip) Hutch). Evidence were gathered using data from direct observations of larval movement and behavior, faeces analysis, scanning electron microscopy of plant surface and experimental analysis of larval movement on plants with and without trichomes (manually removed). The latter involved a comparison with a non specialist congener, Heliconius pachinus Salvin. Observations showed that H. charithonia larvae are capable of freeing themselves from entrapment on trichome tips by physical force. Moreover, wandering larvae lay silk mats on the trichomes and remove their tips by biting. In fact, trichome tips were found in the faeces. Experimental removal of trichomes aided in the movement of the non specialist but had no noticeable effect on the specialist larvae. These results support the suggestion that trichomes are capable of deterring a non specialist herbivore (H. pachinus). The precise mechanisms that allow the success of H. charithonia are not known, but I suggest that a blend of behavioral as well as physical resistance mechanisms is involved. Future studies should ascertain whether larval integument provides physical resistance to trichomes.     

Accessory Pollen Adhesive from Glandular Trichomes on the Anthers of Leonurus sibiricus L. (Lamiaceae)

Abstract: Glandular trichomes (ca. 16 per anther) on the anthers of Leonurus sibiricus produce a secretion that, when touched, is liberated at once and becomes sticky when in contact with the air. With successive visitations of the pollinators (species of Bombus in naturalized populations) the number of secretion‐containing glands on each anther diminishes by mechanical rupture. On the pollinators, the secretion mixed with pollen was found adhered to the integument on the parts making contact with the anthers and stigma, mostly on the scape of the antennae. These trichomes are anatomically identical to the glandular scales common in the entire family and are formed by a multicellular cuticle‐bounded structure, with a foot and head. The secretion is accumulated as a milky emulsion under the cuticle, outside the primary cell wall, and is liberated by rupture of the cuticle. The composition possibly differs from what generally distinguishes these glandular trichomes, i.e. volatile oils that give these plants their particular smell. Such volatile compounds are generally assumed to have defensive or attractive functions, different from those observed in this study, which would be strictly mechanical.     

GYNOECIAL ONTOGENY AND MORPHOLOGY,AND POLLEN TUBE PATHWAY IN BLACK MAPLE,ACER SACCHARUM SSP. NIGRUM (ACERACEAE)

The black maple (Acer saccharum Marsh, ssp. nigrum [Michx. f.] Desm.) gynoecium displays classical involute carpel development; carpels form, in mid- to late-summer, as two separate, opposite, hood-shaped primordia bearing naked megasporangia on inrolled carpel margins. Megasporogenesis, integument initiation, and carpel closure occur in spring; carpels fuse, forming a biloculate ovary with a short, hollow style and two divergent, dry, unicellular papillose stigmas. Transmitting tissues consist of developmentally and morphologically similar trichomes that form along the apparent carpel margins. The path from stigma to micropyle is open, but pollen tubes do not grow entirely ectotrophically. Germinating at the tip of a stigma papilla, a tube grows, apparently under the cuticle, to the papilla base. It then grows between stigma cells to the style, emerging to grow ectotrophically through the style to the compitum, where it passes into one of the locules. Within a locule, the tube grows over placenta and obturator to the micropyle, then between megasporangium cells to the female gametophyte, spreading over the surface near the egg. This study adds to our sparse understanding of gynoecium development and transmitting tissue in relation to pollen tube growth in naturally pollinated woody plants.     

Anatomy,trichome morphology and palynology of Salvia chrysophylla Stapf (Lamiaceae)

The anatomy, palynology, morphology and distribution of the trichomes on the aerial parts of Salvia chrysophylla Stapf, an endemic species in Turkey, were studied in order to understand the usefulness of these characteristics for systematic purposes. Some anatomical characters such as (1–)2–24-rowed pith rays in roots, dorsiventral leaves, obviously larger upper epidermal cells, and two to three large vascular bundles in the center and two to four small subsidiary bundles in the wings of petiole provide information of taxonomical significance. Three main types of trichomes were observed on the stem, inflorescence axis, leaf and calyx surfaces of S. chrysophylla. They are peltate, capitate glandular and non-glandular. Capitate glandular and non-glandular trichomes were further subdivided into several kinds. Glandular trichomes are present in abundance on the inflorescence axis and calyx, but non-glandular ones were mainly situated on the leaf and stem. Scanning Electron Microscopy (SEM) studies on the pollen grains have revealed that they are oblate-spheroidal and their exine ornamentation is bireticulate-perforate.     

Stigma behavior in Mimulus aurantiacus (Scrophulariaceae)

The bilobed stigma of many species in the order Scrophulariales closes in response to touch by an animal pollinator. In hummingbird-pollinated bush monkey flower, Mimulus aurantiacus (Scrophulariaceae), closure is rapid, occurring within seconds of tactile stimulus. We investigated the proximate causes of stigma closure and subsequent reopening in M. aurantiacus, as well as potential costs and benefits of stigma closure for female fitness. Stigma closure is elicited by both touch and pollen, but closure in response to pollen is much slower, requiring 0.5–1.5 h. Stigmata reopen within 2.5–4.5 h if touch, but no pollen, is applied. Upon receipt of pollen, most stigmata remain closed for the remaining lifetime of the flower, even if less pollen is received than is needed for full seed set. Those stigmata that do reopen after pollination generally require between 20 and 28 h to do so, much longer than for unpollinated stigmata. Reopening after pollination appears to be a response to low seed set rather than to low pollen load. Natural pollination of stigmata manipulated to prevent closure shows that closure does not increase capture of pollen or seed set. In fact, closure reduces the average pollen load received by flowers. Despite this, there is no evidence that stigma closure has any negative effect on female fitness in terms of seed set or germinability. Hypotheses for the adaptive significance of stigma closure are discussed. Understanding proximate causes of stigma closure and reopening is essential in the evaluation of these hypotheses.     

Trichome complement of Turnera and Piriqueta (Turneraceae)

The indumentum of Piriqueta and Turnera is made up of nine different types of trichomes, which broadly can be divided into glandular and non-glandular. Taking into account foot shape, head size and pedicle size, five variants of glandular trichomes are recognized: microcrapitate, stipitate-capitate, sessile-capitate and setiform. The non-glandular trichomes can be simple (unicellular or pluricellular-uniseriate), stellate or porrect-stellate. The setiform glandular hairs are present in most species of Piriqueta . Simple unicellular hairs are the most widespread type, frequently being found in combination with other trichomes. Stellate trichomes show a restricted distribution in both genera. Within Piriqueta , section Africana has only simple trichomes, whereas section Piriqueta has also porrect-stellate trichomes; groups of species can be set up according to the presence and type of glandular trichomes. Within Turnera the stipitate-capitate trichomes are exclusive to series Papilliferae ; sessile-capitate trichomes are found in series Microphyllae , Annulares and in some species of Salicifoliae ; clavate trichomes are found only in series Turnera ; setiform glandular hairs are exclusive to T. collotricha , whereas the microcapitate trichomes are widely distributed.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 144 , 85–97.     

Comparative leaf anatomical studies of some Sterculia L. species (Sterculiaceae)

A comparative study was undertaken on the leaves of 12 Sterculia species in order to assess anatomical variations which may be useful in species identification and to evaluate their significance in the taxonomy of the genus. All species have glandular and non-glandular trichomes, anomocytic stomata, multiple and mucilaginous epidermis, mucilaginous cavities and druses in mesophyll tissues. A small amount of variation was observed in the outline of transverse sections of midribs and petioles, the presence of central vascular bundles, and the type of trichomes. Some characters, such as the vertically divided adaxial epidermis in S. macrophylla , are unique to certain species and are therefore useful in diagnostic characters, while S. coccinea and S. elongata appear to be similar in the structure of the petiole and midrib. The results, however, do not show any groupings of species and do not support the observations of others on groups derived from wood anatomy.     

Leaf anatomy of Gluta (L.) Ding Hou (Anacardiaceae)

An anatomical study of the leaves of 21 species of Gluta (L.) Ding Hou (Anacardiaceae) reveals two major groups of species which reflect the original groups of Gluta L. and Melanorrhoea Wall., and a smaller group showing intermediate, or an admixture of, characters. The anatomical characters found to be of most use in this respect are: stomatal outline in surface view; stomatal density; glandular trichomes present/absent; glandular trichome body raised/sunken; cuticle striate/not striate; midrib dimensions as seen in transverse section; kind of simple trichomes (trichome-types 1–4); epidermal cell anticlinal wall undulation and whether visible or not on cuticular surface; resin ducts present/absent in medullary parenchyma of midrib. These characters have been used in a key to the species. Some evidence is given that the lacquer covering the leaf surface of some species is produced by the terminal cells of the glandular trichomes.