Morphological diversity of glandular trichomes in Urticalean Rosids

Nascimento, Isabel Cristina; Leme, Flávia Maria; Teixeira, Simone Pádua

doi:10.1590/0102-33062022abb0061

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Original article • Acta Bot. Bras. 36 • 2022 • https://doi.org/10.1590/0102-33062022abb0061 copy

Morphological diversity of glandular trichomes in Urticalean Rosids

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Glandular trichomes are epidermal structures that produce, store and release a variety of chemical compounds. Their high morphological diversity allows their taxonomic use at various levels. Therefore, their description and standardization of terminology become challenging. Cannabaceae is a well known family of Urticalean Rosids because of the presence of cannabinoid-secreting trichomes in Cannabis sativa. Other Urticalean Rosid families (Moraceae, Ulmaceae and Urticaceae) are neglected in this regard. Thus, the morphology and distribution of glandular trichomes were studied in Cannabaceae and Ulmaceae species and compared with published data for Moraceae and Urticaceae. Surface and anatomical analyses were performed on vegetative and floral organs. Urticalean Rosids show at least 15 types of glandular trichomes, 12 of them capitate and three filiform. In particular, Trema micrantha, a Cannabaceae species, has six different types. A trichome with biseriate stalk and pluricellular head, found in Trema micrantha and Pteroceltis tatarinowii, was not previously reported. Glandular trichomes are widely distributed in the plant body, which may be related to protection against herbivory. The greatest difficulty was the large quantity of terms and the lack of morphological details of the glandular trichomes in previous studies. A standardization of the terminology of glandular trichomes was therefore proposed.

Keywords:
anatomy; Cannabaceae; Moraceae; terminology; Ulmaceae; Urticaceae

Introduction

Glandular trichomes are epidermal appendages responsible for the production, storage and release of a variety of chemical compounds (Esau 1977Esau K. 1977. Anatomy of seed plants. New York, John Wiley & Sons.; Fahn 1979Fahn A. 1979. Secretory tissues in plants. New York, Academic Press.). They are formed by a portion inserted into the epidermis, called base, and a segment that is above the surface of the epidermis, called stalk, which may be single or pluricellular, single or multiseriate, or even absent (Fahn 1979Fahn A. 1979. Secretory tissues in plants. New York, Academic Press.; Dickinson 2000Dickinson WG. 2000. Integrative Plant Anatomy. San Diego, Academic Press.; Cutler et al. 2008Cutler DF, Botha T, Stevenson DW. 2008. Plant anatomy: an applied approach. Oxford, Blackwell Publishing. ). In the apical portion of the trichome there is a secretory head, which may be uni- or pluricellular (Fahn 1979Fahn A. 1979. Secretory tissues in plants. New York, Academic Press.; Cutler et al. 2008Cutler DF, Botha T, Stevenson DW. 2008. Plant anatomy: an applied approach. Oxford, Blackwell Publishing. ).

Glandular trichomes are of great importance for the systematic investigation of angiosperms, with a few species being devoid of this type of structure (Fahn 1988Fahn A. 1988. Secretory tissues in vascular plants. New Phytologist 108: 229-257.; Metcalfe & Chalk 1950Metcalfe CR, Chalk L. 1950. Anatomy of the Dicotyledons. Vol. 2. Clarendon Press, Oxford.; Wagner 1991Wagner GJ .1991. Secreting glandular trichomes: more than Just hairs. Plant Physiology 96: 675-679.; Duke 1994Duke SO. 1994. Glandular trichomes - a focal point of chemical and structural interactions. International Journal of Plant Sciences 155: 617-620.; Beck 2005Beck CB. 2005. An introduction to plant structure and development. Cambridge, Cambridge University Press.). The number and arrangement of the cells forming the stalk and the head result in several morph types of trichomes that are important for plant systematics (Payne 1978Payne WW. 1978. A glossary of plant hair terminology. Brittonia 30: 239-255. ; Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; Azizian 2002Azizian D. 2002. Morphology and distribution of trichomes in some genera (Morus, Ficus, Broussonetia and Maclura). Iranian Journal of Botany 9: 195-202.; Marquiafável et al. 2009Marquiafável FS, Ferreira MDS, Teixeira SP. 2009. Novel reports of glands in Neotropical species of Indigofera L. (Leguminosae, Papilionoideae). Flora 204: 189-197.; Vargas et al. 2019Vargas W, Fortuna-Perez AP, Lewis GP, Piva TC, Vatanparast M, Machado SR. 2019. Ultrastructure and secretion of glandular trichomes in species of subtribe Cajaninae Benth (Leguminosae, Phaseoleae). Protoplasma 256: 431-445.). Proper identification of glandular trichomes requires investigation of important aspects such as macromorphology, anatomy, and chemical composition of the exudate (Theobald et al. 1979Theobald WL, Krahulink JL, Rollins RC. 1979. Trichome descriptions and classification. In: Metcalfe CR, Chalk L. (Ed.) Anatomy of the Dicotyledons. Vol.1. Oxford, Science Publications., Azizian 2002Azizian D. 2002. Morphology and distribution of trichomes in some genera (Morus, Ficus, Broussonetia and Maclura). Iranian Journal of Botany 9: 195-202.; Marquiafável et al. 2009Marquiafável FS, Ferreira MDS, Teixeira SP. 2009. Novel reports of glands in Neotropical species of Indigofera L. (Leguminosae, Papilionoideae). Flora 204: 189-197.; Vargas et al. 2019Vargas W, Fortuna-Perez AP, Lewis GP, Piva TC, Vatanparast M, Machado SR. 2019. Ultrastructure and secretion of glandular trichomes in species of subtribe Cajaninae Benth (Leguminosae, Phaseoleae). Protoplasma 256: 431-445.).

Cannabaceae is a prominent family known for its medicinal potential regarding cannabinoid production in the glandular trichomes of Cannabis sativa (Furr & Mahlberg 1981Furr M, Mahlberg PG. 1981. Histochemical analyses of laticifers and glandular trichomes in Cannabis sativa. Journal of Natural Products 44: 153-159.). These glandular trichomes have been extensively studied for morphology, distribution and exudate composition. However, the wide diversity of glandular trichomes in the family (Hammond & Mahlberg 1973Hammond CT, Mahlberg PG. 1973. Morphology of glandular hairs of Cannabis sativa from scanning electron microscopy. American Journal of Botany 60: 524-528.; 1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.; Gangadhara & Inamdar 1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.; Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; St-Laurent et al. 2000St-Laurent L, Baum BR, Akpagana K, Arnason JT. 2000. Leaf trichome morphology and density in West African Trema spp. (Ulmaceae: Celtidoideae). Canadian Journal of Botany 78: 34-39.) has not yet been cataloged. Ulmaceae, the elm family closely related to Cannabaceae, also exhibits glandular trichomes (Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; Leme et al. 2018Leme FM, Staedler YM, Schonenberger J, Teixeira SP. 2018. Ontogeny and vascularization elucidate the atypical floral structure of Ampelocera glabra, a tropical species of Ulmaceae. International Journal of Plant Science 179: 461-476.), which, however, have been little studied in terms of morphology, distribution and exudate composition.

The circumscription of Cannabaceae and Ulmaceae was changed by molecular data, with genera previously belonging to Ulmaceae being transferred to Cannabaceae (Sytsma et al. 2002Sytsma KJ, Morawetz J, Pires JC, et al. 2002. Urticalean rosids: circumscription, rosid ancestry, and phylogenetics based on rbcL, trnLF, and ndhF sequences. American Journal of Botany 89: 1531-1546.). These two families, together with Urticaceae and Moraceae, form the Urticalean clade of rosids (Sytsma et al. 2002Sytsma KJ, Morawetz J, Pires JC, et al. 2002. Urticalean rosids: circumscription, rosid ancestry, and phylogenetics based on rbcL, trnLF, and ndhF sequences. American Journal of Botany 89: 1531-1546.), a group with some registers of glandular trichomes (Gangadhara & Inamdar 1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.; Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; Schnetzler et al. 2017Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.). Different terms are often used (see Briosi & Togni 1894Briosi G, Tognini F. 1894. Anatomia Della Canapa (Cannabis sativa L.). Milano, Istituto Botanico Della R, Universitá Di Pavia.; Dayanandan & Kaufman 1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.; Gangadhara & Inamdar 1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.; Hammond & Malhberg 1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.; Oliveira et al. 1988Oliveira MM, Salomk M, Pais M. 1988. Glandular trichomes of Humulus lupulus var. Brewer’s Gold: ontogeny and histochemical characterization of the secretion. Nordic Journal Botany 8: 349-359.; Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.), with the study of the morphology of trichomes in this group being a challenge.

Thus, the objective of the present study was to investigate the distribution and morphology of the glandular trichomes of three species of Cannabacae and four species of Ulmaceae (see Tab. 1) and compare them with published data for Moraceae and Urticaceae. We intended to elaborate a set of taxonomic characteristics for this group of plants and also to contribute to the standardization of a more appropriate terminology for glandular trichomes in general. The lack of standardization of terms for the glandular trichomes prevents comparative studies, thus hampering the use of these structures as support for taxonomic studies.

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Table 1
Information on the Cannabaceae and Ulmaceae species analysed in the present study.

Materials and methods

Samples of the vegetative and reproductive organs of seven species of Cannabaceae and Ulmaceae were collected at different locations (Tab. 1). Two to three individuals were sampled for each species. Vouchers were deposited in the SPFR herbarium (FFCLRP/USP, Ribeirão Preto, Brazil) and in the CGMS herbarium (UFMS, Campo Grande, Brazil) (Tab. 1).

The material was fixed in FNT (buffered formalin; Lillie 1965) or in FAA (formalin, acetic acid, and 50 % ethanol) (Johansen 1940Johansen DA. 1940. Plant Microtechnique. New York and London, McGraw-Hill.) for 24 hours, washed in water or 50 % ethanol, respectively, dehydrated in an ethanol series up to 70 % and then processed for analysis of distribution and external morphology of the trichomes by scanning electron microscopy (SEM), and of anatomy by light microscopy (LM).

For surface analysis (SEM), samples were dehydrated in an ethanol series up to absolute alcohol and dried at CO₂ critical point in a Bal-Tec CPD 030 apparatus. Next, they were mounted on metal supports with carbon adhesive tape, coated with gold with a Bal-Tec SCD 050 sputter-coater and observed with a Zeiss EVO-50 scanning electron microscope at 15 kv.

For the anatomical study (LM), samples were dehydrated in an ethanol series up to absolute alcohol, embedded in histological resin (Leica) and cut into 3 to 6 µm-thick sections on transverse and longitudinal planes using a rotary microtome (Leica RM2245). The sections were stained with 0.05 % toluidine blue, pH 4.4 or 5.8 (O’Brien et al. 1964O’Brien TP, Feder N, McCully ME. 1964. Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59: 367-373.), Sudan III, and Sudan Black B (Pearse 1972Pearse AG. 1972. Histochemistry: theoretical and applied. 3a ed. Baltimore, The Williams & Wilkins Company.) for observation of cutin and suberin in the cell wall.

We used the functions prcomp and autoplot (ggfortify package) in the R computational environment (R Development Core Team 2020R Development Core Team. 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.) to run the principal component analysis (PCA). The dataset consisted of 56 lines representing the species and 15 columns representing the glandular trichome types. For each species we computed the number of organs each glandular trichome type occurred (i.e., sepal, leaf or stem).

The glandular trichomes were classified according to Payne's glossary (1978Payne WW. 1978. A glossary of plant hair terminology. Brittonia 30: 239-255. ) and by comparison with trichomes described in the literature for Cannabaceae and Ulmaceae species (Briosi & Togni 1894Briosi G, Tognini F. 1894. Anatomia Della Canapa (Cannabis sativa L.). Milano, Istituto Botanico Della R, Universitá Di Pavia.; Dayanandan & Kaufman 1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.; Gangadhara & Inamdar 1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.; Hammond & Malhberg 1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.; Oliveira et al. 1988Oliveira MM, Salomk M, Pais M. 1988. Glandular trichomes of Humulus lupulus var. Brewer’s Gold: ontogeny and histochemical characterization of the secretion. Nordic Journal Botany 8: 349-359.; Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; Leme et al. 2018Leme FM, Staedler YM, Schonenberger J, Teixeira SP. 2018. Ontogeny and vascularization elucidate the atypical floral structure of Ampelocera glabra, a tropical species of Ulmaceae. International Journal of Plant Science 179: 461-476.; Leme et al. 2020Leme FM, Schönenberger J, Staedler YM, Teixeira SP. 2020. Comparative floral development reveals novel aspects of structure and diversity of flowers in Cannabaceae. Botanical Journal of Linnean Society 193: 64-83.).

In an attempt to standardize their terminology, glandular trichomes were denoted as capitate if there was a distinction between head and stalk, and filiform if there was no such distinction. Capitate trichomes were defined as uni-, bi-, or pluricellular and as uni-, bi-, or multiseriate considering the number of stalk cells, and as uni- or pluricellular considering the number of head cells. In addition, the filiform type of trichome was defined as uni- or biseriate considering the number of cell series and the total number of cells. Descriptions, schemes and images available in the literature were checked for such standardization.

Results

The data collected in the present study and those found in the literature accounted for 15 different glandular trichome morph types in Cannabaceae, Moraceae, Ulmaceae and Urticaceae, described and organized in Table 2. Among these 15 types of glandular trichomes, five types were found in the sampled species of Cannabaceae and Ulmaceae in this study (Tab. 3) and were first assigned to two large groups, i.e., capitate (Fig. 1) and filiform (Fig. 2).

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Table 2
Types and distribution of glandular trichomes in the analysed species of Cannabaceae and Ulmaceae. Symbols: + = present; - = absent; empty cell = without information.

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Table 3
Types of glandular trichomes found in the present study and described in the literature for other Urticalean Rosids.

Figure 1
Capitate trichomes of Cannabaceae and Ulmaceae species (SEM). A. Capitate trichome with a uniseriate and pluricellular stalk and pluricellular head, Celtis pubescens (type 3). B. Capitate trichome with a biseriate stalk and pluricellular head, Trema micrantha (type 12). C. Capitate trichome with a unicelular stalk and pluricellular head, Ampelocera glabra (type 6).

Figure 2
Filiform trichomes of Cannabaceae species (SEM). A. Filiform uniseriate trichome, Celtis pubescens (type 14). B. Filiform biseriate trichome with six to eight cells, Trema micrantha (type 15).

Capitate glandular trichomes

Three types of capitate glandular trichomes are found and classified according to descriptions of Table 2.

Capitate trichome with a uniseriate, four- to eight-celled stalk, multiseriate and pluricellular head (Figs. 1A, 3A-C). It occurs on the young stem, on the petiole, on both surfaces of the leaf blade (Fig. 3E), on the pedicel (Fig. 3F), and on the abaxial surfaces of the sepals only in Celtis pubescens (Cannabaceae) (type 3 - Tabs. 2, 3).

Figure 3
Capitate glandular trichomes (type 3) of Celtis pubescens (Cannabaceae). A. Longitudinal section showing the uniseriate stalk and pluricellular head (LM). B. Head cells after exudate release (SEM). C. Distribution of trichomes on the abaxial side of the leaf blade (SEM). D. Distribution of trichomes on the pedicel (SEM).

Capitate trichome with a biseriate stalk, each series with four to six cells, and a six- to eight-celled head (Figs. 1B, 4A-B). It occurs on the young stem, on the petiole, and on both sides of the leaf blade, predominantly on the abaxial side and on the midrib (Fig. 4D) in Trema micrantha and Pteroceltis tatarinowii (Cannabaceae). In the floral organs, it occurs on the pedicel only in T. micrantha (Fig. 4E), on the abaxial side of the sepals of T. micrantha and P. tatarinowii, and on the pistil of P. tatarinowii (type 12 - Tabs. 2, 3).

Capitate trichome with a unicellular stalk and a four-celled head (Figs. 1C, 5A, C-G). It occurs on the young stem, petiole, and on both sides of the leaf blade, predominantly on the abaxial side and on the midrib of Ampelocera glabra, Phyllostylon rhamnoides, Ulmus parvifolia and Zelkova serrata (Fig. 5B, D, F, H). In the floral organs it occurs on the sepals of A. glabra and on the pistil of A. glabra and Z. serrata (type 6 - Tabs. 2, 3).

Figure 4
Capitate glandular trichomes (type 12) of Cannabaceae species. A. Biseriate and pluricellular stalk and pluricellular head, Pteroceltis tatarinowii (SEM). B-E. Trema micrantha. B. Longitudinal section of the capitate trichome with a biseriate stalk and pluricellular head (LM). C. Detail of the trichome head after exudate release; note that there is no cell disruption (SEM). D. Distribution of trichomes on the adaxial side of the leaf blade (SEM). E. Distribution of glandular trichomes on the pedicel among numerous simple trichomes (SEM).

Figure 5
Capitate glandular trichomes (type 6) with a unicellular stalk and pluricellular head of Ulmaceae species (SEM). A-B. Ampelocera glabra. A. Detail. B. Distribution of trichomes on the abaxial side of the leaf blade. C-D. Phyllostylon rhamnoides. C. Detail. D. Distribution of trichomes on the abaxial side of the leaf blade. E-F. Ulmus parvifolia. E. Detail. F. Distribution of trichomes on the abaxial side of the leaf blade. G-H. Zelkova serrata. G. Trichome after release of the exudate; note that there is no disruption of cells. H. Distribution of trichomes on the ovary.

Filiform glandular trichomes

Two types of filiform glandular trichomes are found and classified according to descriptions of Table 2.

Uniseriate, six- to eight-celled filiform trichome (Figs. 2A, 6A). It occurs only in Celtis pubescens (Cannabaceae) on the young stem, on the petiole, and on both sides of the leaf blade (Fig. 6C), more densely distributed on the abaxial side and midrib, on the pedicel (Fig. 6D), and on the abaxial side of the sepals (type 14 - Tabs. 2, 3).

Biseriate filiform trichome, with six to eight cells in each series (Figs. 2B, 7A). It occurs only in Trema micrantha (Cannabaceae) on the young stem, petiole, on both sides of the leaf blade, more densely distributed on the abaxial side and midrib (Fig. 7C), on the pedicel (Fig. 7D), and on the abaxial side of the sepals (type 15 - Tabs. 2, 3).

All types of glandular trichomes found in the sampled species release the exudate with no evidence of disintegration of the secretory cells but with loss of turgidity characterizing a granulocrine type of secretion (Figs. 3B, 4C, 4D, 5G, 6B).

Figure 6
Uniseriate filiform trichomes (type 14) of Celtis pubescens, Cannabaceae (SEM). A. Apical cells before exudate release. B. Apical cells after exudate release. C. Distribution of trichomes on the midrib of the leaf blade on the abaxial side. D. Trichome on the pedicel.

Figure 7
Biseriate filiform trichomes (type 15) of Trema micrantha, Cannabaceae. A. Longitudinal section of a trichome showing apical cells with densely stained cytoplasm and a large central nucleus (LM). B. Trichome in the process of exudate release; note that the cells lose their turgidity (SEM). C. Distribution of trichomes on the leaf blade among simple trichomes (SEM). D. Distribution of trichomes on the flower pedicel (SEM).

Principal Component Analysis (PCA)

The first three PCA axes explained 42.1 % of the data variance. The first axis separated Moraceae and Urticaceae species from the others especially by the presence of glandular trichomes of types 1 (capitate with a unicellular head), 5 (capitate with a bicellular head) and 6 (capitate with a pluricellular head) (Fig. 8, Tab. 2). The second and third axes separated Cannabaceae species from the others especially by the presence of glandular trichomes of types 8 (capitate with a four to eight-celled head), 9 (capitate with a disc-shaped head), 12 (capitate with a biseriate pluricellular stalk and pluricellular head), 14 (uniseriate filiform) and 15 (biseriate filiform) (Fig. 8, Tab. 2).

Figure 8
Biplot of axes 1 and 2 (A), and of axes 2 and 3 (B) of the species ordenation according to glandular trichome types and their distribution in the plant body.

Discussion

Urticalean Rosids exhibit a great morphological diversity of glandular trichomes, with at least 15 different morph types described and grouped into capitate and filiform types (see Tab. 2). Cannabaceae, the most economically important family in the group, is also the most diverse family in terms of types of glandular trichomes (10 morph types), seven of the capitate type and three of the filiform type (Tab. 3). This is probably due to the greater number of studies carried out with Cannabis sativa and Humulus lupulus (Briosi & Togni 1894Briosi G, Tognini F. 1894. Anatomia Della Canapa (Cannabis sativa L.). Milano, Istituto Botanico Della R, Universitá Di Pavia.; Dayanandan & Kaufman 1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.; Gangadhara & Inamdar 1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.; Hammond & Malhberg 1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.; Oliveira et al. 1988Oliveira MM, Salomk M, Pais M. 1988. Glandular trichomes of Humulus lupulus var. Brewer’s Gold: ontogeny and histochemical characterization of the secretion. Nordic Journal Botany 8: 349-359.; Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; present study). The least diverse family is Urticaceae with three morph types, an unexpected finding compared to the number of species included in each family (1422 spp. in Urticaceae versus 110 spp. in Cannabaceae, Yang et al. 2013Yang MQ, van Velzen R, Bakker FT, Sattarian A, Li DZ, Yi TS. 2013. Molecular phylogenetics and character evolution of Cannabaceae. Taxon 62: 473-485.; The Plant List 2013The Plant List. 2013. Version 1.1. http://www.theplantlist.org/. 21 Aug. 2018.
http://www.theplantlist.org/... ). We must consider that this family has been subsampled, as shown in Table 3 (only seven species with records of glandular trichomes), or that it is noteworthy by the presence of “stinging trichomes” (Fu et al. 2003Fu HY, Chen SJ, Huang LLK. 2003. Comparative study on the stinging trichomes and some related epidermal structure in the leaves of Dendrocnide meyeniana, Girardinia diversifolia, and Urtica thunbergiana. Taiwania 48: 213-223.) that actually are stinging emergences (Evert 2006Evert RF. 2006. Esau's Plant Anatomy: Meristems, Cells, and Tissues of the Plant Body: Their structure, function, and development. 3rd ed. New Jersey, Wiley-Interscience.). In Ulmaceae, a family comprising 64 species (The Plant List 2013The Plant List. 2013. Version 1.1. http://www.theplantlist.org/. 21 Aug. 2018.
http://www.theplantlist.org/... ), five morph types of glandular trichomes were found, three of them of the capitate type and two of the filiform type (Tabs. 2, 3). Morph type 6 (capitate trichome with a unicellular stalk and pluricellular head) had already been reported for other species of this family (Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; Tab. 2) and could be considered to be a unifying feature for the group. However, taking into account that species of Moraceae exhibit similar glandular trichomes with pluricellular heads (Schnetzler et al. 2017Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.), this morph type cannot be considered a diagnostic characteristic for Ulmaceae.

Trema Lour. was the Cannabaceae genus with the highest number of morph types (six) found, followed by Celtis (three) and Cannabis (three). Other genera such as Humulus, Lozanella, Chaetachme, Parasponia and Pteroceltis have one or two trichome morph types (Tab. 2). The previously unreported result of our study is the description of the capitate glandular trichome (morph type 12) found in Trema micrantha and Pteroceltis tatarinowii, which has a biseriate stalk and a pluricellular head. A glandular trichome with a biseriate stalk is a rare condition found in Cannabaceae (Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.) or even throughout the Urticalean Rosids, with records only for Cannabis sativa (Dayanandan & Kaufman 1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.; Hammond & Mahlberg 1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.) and Humulus lupulus (Oliveira et al. 1988Oliveira MM, Salomk M, Pais M. 1988. Glandular trichomes of Humulus lupulus var. Brewer’s Gold: ontogeny and histochemical characterization of the secretion. Nordic Journal Botany 8: 349-359.). The two morph types found in Celtis pubescens (Gangadhara & Inandar 1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.; Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; present study), as well as the filiform morph type found in Trema micrantha (Bhat & Kachroo 1979Bhat MM, Kachroo P. 1979. The trichome in phylogeny of Urticales. Annual Reviews of Plant Sciences 1: 375-407., apudTobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.) had been previously reported.

It is noteworthy that the different glandular trichome morph types of Cannabaceae species can occur in the same organ (Tabs. 2, 3). This wide distribution in the plant body (leaf, stem, pedicel, ovary), also observed in other Urticalean Rosids (Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; Shah & Kachroo 1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.; Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.; Sugiyama et al. 2006Sugiyama R, Oda H, Kurosaki F. 2006. Two distinct phases of glandular trichome development in hop (Humulus lupulus L.). Plant Biotechnology 23: 493-496.; Schnetzler et al. 2017Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.; Tab. 3), may be related to plant protection against herbivory (Loe et al. 2007Loe G, Torang P, Gaudeul M, Âgren J. 2007. Trichome production and spatiotemporal variation in herbivory in the perennial herb Arabidopsis lyrata. Oikos 116: 134-142.) since many of these species are wind pollinated (Judd et al. 2009Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ. 2009. Sistemática Vegetal - Um enfoque filogenético. Porto Alegre, Artmed.), meaning that such glandular trichomes would not be involved in the attraction of pollinating animals. The defense against herbivory has been previously reported for Cannabis sativa in which the action of chemical compounds secreted by trichomes occurs when the herbivore disrupts trichome head cells (Small & Naraime 2016Small E, Naraine SGU. 2016. Size matters: evolution of large drug-secreting resin glands in elite pharmaceutical strains of Cannabis sativa (marijuana). Genetic Resources and Crop Evolution 63: 349-359.). In some cases, the released compounds may trap small insects and, in the case of larger insects, trichomes may release sticky substances with an unpleasant odor and/or taste, which would discourage herbivory (Small & Naraime 2016Small E, Naraine SGU. 2016. Size matters: evolution of large drug-secreting resin glands in elite pharmaceutical strains of Cannabis sativa (marijuana). Genetic Resources and Crop Evolution 63: 349-359.).

Interestingly, the capitate types of glandular trichome described here for species of Cannabaceae and Ulmaceae are very different; those of Ulmaceae are smaller (around 40 to 50 µm vs. 40 to 100 µm in Cannabaceae species), mainly due to their uni- or bicellular stalk. However, it is difficult to propose explanations for such a difference that could be related to: (a) different chemical composition of the exudate in each family and (b) need for organ protection in a family whose members are diverse in terms of habits, as occurs in Cannabaceae (trees, shrubs, herbs or lianas - Judd et al. 2009Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ. 2009. Sistemática Vegetal - Um enfoque filogenético. Porto Alegre, Artmed.).

The differences observed in the types of glandular trichomes found in the species of Cannabaceae and Ulmaceae (see Fig. 8) support the new circumscription of Celtis, Pteroceltis and Trema in Cannabaceae (previously inserted in Ulmaceae) (Sytsma et al. 2002Sytsma KJ, Morawetz J, Pires JC, et al. 2002. Urticalean rosids: circumscription, rosid ancestry, and phylogenetics based on rbcL, trnLF, and ndhF sequences. American Journal of Botany 89: 1531-1546.). These genera stand out for being the species-richest in the family (Yang et al. 2013Yang MQ, van Velzen R, Bakker FT, Sattarian A, Li DZ, Yi TS. 2013. Molecular phylogenetics and character evolution of Cannabaceae. Taxon 62: 473-485.). Similar inferences can be found in Metcalfe & Chalk (1950Metcalfe CR, Chalk L. 1950. Anatomy of the Dicotyledons. Vol. 2. Clarendon Press, Oxford.), Narayana (1979Narayana BM. 1979. Taxonomic value of trichomes in Vernonia Schreb (Asteraceae). Proceedings of the Indian National Science Academy 88: 347-357.), Adedeji et al. (2007Adedeji O, Ajuwon OY, Babawale OO. 2007. Foliar epidermal studies, organographic distribution and taxonomic importance of trichomes in the family Solanaceae. International Journal of Botany 3: 276-282.). The diverse morphology and distribution of glandular trichomes allow their use in plant systematics, especially in the diagnosis of genera (Narayana 1979Narayana BM. 1979. Taxonomic value of trichomes in Vernonia Schreb (Asteraceae). Proceedings of the Indian National Science Academy 88: 347-357.; Adedeji et al. 2007Adedeji O, Ajuwon OY, Babawale OO. 2007. Foliar epidermal studies, organographic distribution and taxonomic importance of trichomes in the family Solanaceae. International Journal of Botany 3: 276-282.) or even of families, such as Lamiaceae (Metcalfe & Chalk 1950Metcalfe CR, Chalk L. 1950. Anatomy of the Dicotyledons. Vol. 2. Clarendon Press, Oxford.). However, the lack of homogeneity in terms and descriptions makes it difficult to infer about the taxonomic value of glandular trichomes, which can be exemplified by Cannabaceae. Thus, our proposed standardization of terminology for glandular trichomes reported for Cannabaceae and Ulmaceae (see Tab. 2) is essential. Some examples are given below.

Capitate trichomes as considered in the present study based on an evident distinction between the stalk and head cells have been reported in the literature as bulbous trichomes (spherical head) or as peltate trichomes (flat head) (Sugiyama et al. 2006Sugiyama R, Oda H, Kurosaki F. 2006. Two distinct phases of glandular trichome development in hop (Humulus lupulus L.). Plant Biotechnology 23: 493-496.). Bulbous trichomes have been reported to have different cell numbers: 1-2 stalk cells, 1-2, 4 head cells (Hammond & Mahlberg 1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.; Oliveira & Pais 1988Oliveira MM, Salomk M, Pais M. 1988. Glandular trichomes of Humulus lupulus var. Brewer’s Gold: ontogeny and histochemical characterization of the secretion. Nordic Journal Botany 8: 349-359.), one-celled stalk and head (Gangadhara & Inamdar 1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.), or two-celled stalk and four-celled head (Dayanandan & Kaufman 1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.). We classified these trichomes into two morph types for C. sativa (see trichomes 1 and 8 in Tab. 2). Most surprisingly, the term bulbous is also used for the stinging trichome of Urticaceae, not discussed in this study because it is actually a secretory emergence (Evert 2006Evert RF. 2006. Esau's Plant Anatomy: Meristems, Cells, and Tissues of the Plant Body: Their structure, function, and development. 3rd ed. New Jersey, Wiley-Interscience.). The peltate trichome has been described for Cannabis sativa and Humulus lupulus as two different morph types based on their distribution on the plant organs (Hammond & Mahlberg 1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.; Sugiyama et al. 2006Sugiyama R, Oda H, Kurosaki F. 2006. Two distinct phases of glandular trichome development in hop (Humulus lupulus L.). Plant Biotechnology 23: 493-496.). Nevertheless, these morph types are morphologically similar in terms of stalk and head composition. Another issue to be considered is the origin of the stalk in the peltate trichome of Cannabis sativa, formed from hypodermal and epidermal cells (Dayanandan & Kaufman 1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.). Thus, we unified these two types into one morph type based on their ontogeny and final structure (Dayanandan & Kaufman 1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.) (see trichome 9 in Tab. 2). Peltate trichomes have also been described for Moraceae as having a head with radially arranged cells and a unicellular (see trichome 10 in Tab. 2, Jacomassi et al. 2010Jacomassi E, Moscheta IS, Machado SR. 2010. Morfoanatomia e histoquímica de órgãos reprodutivos de Brosimum gaudichaudii (Moraceae). Brazilian Journal of Botany 33: 115-129.; Schnetzler et al. 2017Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.) or bicellular stalk (see trichome 11 in Tab. 2, Shah & Kachroo 1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.).

Other types of capitate trichomes comprise those with a multicellular, uniseriate stalk (see trichomes 2, 3 and 4 in the Tab. 2), occurring in Cannabaceae, Ulmaceae (Gangadhara & Inamdar 1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.; present study) and in Moraceae species (Shah & Kchroo 1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.). Our analysis showed that capitate trichomes with a uniseriate head and stalk are typical of Cannabaceae and Ulmaceae species (see Fig. 8). Similar data were obtained for filiform trichomes (see trichomes 13 and 14 in Tab. 2).

Filiform trichomes, here described as having no apparent distinction between the stalk and the head, have been reported as short or long clavate trichomes: short when they have up to four linearly arranged cells and long when they have more than four cells (Tobe & Takaso 1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.). The short clavate trichome is usually found in Ulmaceae species while the long clavate trichome is found more frequently in Cannabaceae species (see Tab. 2). The exceptions are Ampelocera (Ulmaceae) and Lozanella (Cannabaceae), which have long clavate and short clavate trichomes, respectively, probably because both genera are positioned most basally in the phylogeny. Ampelocera is a sister group of the rest of Ulmaceae species (Neubig et al. 2012Neubig K, Herrera F, Manchester SR, Abbott JR. 2012. Fossils, biogeography and dates in an expanded phylogeny of Ulmaceae. Botany 2012: Annual Meeting of the Botanical Society of America in Columbus, Ohio, USA.) and Lozanella is among the most basal genera of Cannabaceae species (Yang et al. 2013Yang MQ, van Velzen R, Bakker FT, Sattarian A, Li DZ, Yi TS. 2013. Molecular phylogenetics and character evolution of Cannabaceae. Taxon 62: 473-485.).

It is important to emphasize that Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.) published a very good anatomical description of trichomes in Urticalean Rosids. However, their terminology is confused because they categorized a similar morphological trichome into two morph types, for example: “Capitate uniseriate filiform stalk with unicellular, bicellular or multicellular head” and “Uniseriate glandular head with uniseriate filiform stalk”. Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.) also published an excellent study using terms such as capitate, peltate, long-clavate and short-clavate for glandular trichomes. We added some information to those descriptions and also demonstrated a greater diversity of trichomes in Cannabaceae than in Ulmaceae.

Considering that new morph types of glandular trichomes continue to be described for Cannabaceae, it is important to improve efforts regarding this topic for Urticalean Rosids as a whole.

Acknowledgements

We thank Edimárcio da Silva Campos (FCFRP/USP), Maria Dolores Seabra Ferreira and José Augusto Maulin (FMRP/USP) for technical assistance, Rodrigo A. Santinelo Pereira for helping with principal component analysis and Elettra Greene for English revision. This work was supported by Sao Paulo Research Foundation (FAPESP - grant numbers 2014/07453-3 and 2018/03691-8), National Council for Scientific and Technological Development (CNPq - grant numbers 302806/2019-9; 156025/2017-5) and Coordination for the Improvement of Higher Education Personnel (CAPES - finance code 001).

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Publication Dates

Publication in this collection
07 Oct 2022
Date of issue
2022

History

Received
15 Mar 2022
Accepted
17 June 2022

This is an open-access article distributed under the terms of the Creative Commons Attribution License

Family	Species	Organ analysed	Sample source	Voucher
Cannabaceae	Celtis pubescens (Kunth) Spreng.	Stem, leaf, sepal, stamen and pistil	USP campus, Ribeirão Preto, SP, Brazil.	F. M. Leme 98 (SPFR)
	Pteroceltis tatarinowii Maxim.	Stem, leaf, sepal, stamen and pistil	Botanical Garden, University of Vienna, Vienna, Austria.	F. M. Leme 128 (CGMS)
	Trema micrantha (L.) Blume	Stem, leaf, sepal, stamen and pistil	USP campus, Ribeirão Preto, SP, Brazil.	F. M. Leme 94, 97, 101(SPFR)
Ulmaceae	Ampelocera glabra Kuhlm.	Stem, leaf, sepal, stamen and pistil	Reserva Particular do Patrimônio Natural (RPPN), Serra do Teimoso, Jussari, BA, Brazil.	F. M. Leme 102, 112 (SPFR)
	Phyllostylon rhamnoides J. Poiss.) Taub.	Stem and leaf	Assentamento Andalúcia, Nioaque, MS, Brazil.	F. M. Leme 109 (SPFR)
	Ulmus parvifolia Jacq.	Stem and leaf	Horto medicinal of the FCFRP, USP campus, Ribeirão Preto, SP, Brazil.	F. M. Leme & I. C. Nascimento (Spirit Collection of FCFRP/USP)
	Zelkova serrata (Thunb.) Makino	Stem, leaf, sepal, stamen and pistil	Botanical Garden, University of Vienna, Vienna, Austria.	F. M. Leme 124 (CGMS)

Trichome type and description	Family	Species	Organ analysed	Reference
Capitate: unicellular stalk, unicellular head	Cannabaceae	Cannabis sativa L.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
	Moraceae	Ficus carica L.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus heterophylla L. f.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus hispida L.f.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus religiosa L.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Maclura pomifera (Raf.) C.K.	Leaf	Hardin (1981Hardin JW. 1981. Atlas of surface features in woody plants, II. Broussonetia, Morus, and Maclura of North America. Bulletin of the Torrey Botanical Club 108: 338-346.)
		Morus alba L.	Leaf	Hardin (1981Hardin JW. 1981. Atlas of surface features in woody plants, II. Broussonetia, Morus, and Maclura of North America. Bulletin of the Torrey Botanical Club 108: 338-346.)
		Morus microphylla Buckley	Leaf	Hardin (1981Hardin JW. 1981. Atlas of surface features in woody plants, II. Broussonetia, Morus, and Maclura of North America. Bulletin of the Torrey Botanical Club 108: 338-346.)
		Morus nigra L.	Leaf	Hardin (1981Hardin JW. 1981. Atlas of surface features in woody plants, II. Broussonetia, Morus, and Maclura of North America. Bulletin of the Torrey Botanical Club 108: 338-346.)
		Morus rubra L.	Leaf	Hardin (1981Hardin JW. 1981. Atlas of surface features in woody plants, II. Broussonetia, Morus, and Maclura of North America. Bulletin of the Torrey Botanical Club 108: 338-346.)
	Urticaceae	Boehmeria caudata Sw.	Leaf	*Fernandez et al. (2011*Fernandez RD, Cabrera CN, Albornoz PL, Arias ME. 2011. Anatomía foliar de Boehmeria caudata (Urticaceae) em la provincia de Tucumán, Argentina. Lilloa 48: 53-59.)
		Fleurya interrupta (L.) Gaudich.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Urtica dioica L.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
Capitate: uniseriate filiform stalk, unicellular head	Cannabaceae	Celtis sp.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
	Cannabaceae	Trema orientalis (L.) Blume	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
	Ulmaceae	Holoptelea integrifolia Planch.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
Capitate: uniseriate stalk, pluricellular head	Cannabaceae	Celtis pubescens Spreng	Stem, leaf, flower	This study
	Cannabaceae	Trema orientalis (L.) Blume	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
	Moraceae	Morus alba L.	Leaf	Shah & Kachro (1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.)
Capitate: uniseriate stalk, bicellular head	Cannabaceae	Trema orientalis (L.) Blume	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
Capitate: uniseriate stalk, bicellular head	Ulmaceae	Holoptelea integrifolia Planch.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
Capitate: unicellular stalk, bicellular head	Moraceae	Dorstenia cayapia Vell.	Leaf	*Schnetzler et al. (2017*Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.)
		Dorstenia indica Wight	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus asperrima Roxb.	Leaf	Gangadhara and Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus heterophylla L. f.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus hispida L. f.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus racemosa L.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Maclura pomifera (Raf.) C.K. Schneid.	Leaf	Azizian (2002)Azizian D. 2002. Morphology and distribution of trichomes in some genera (Morus, Ficus, Broussonetia and Maclura). Iranian Journal of Botany 9: 195-202.
		Morus alba L.	Leaf	Azizian (2002)Azizian D. 2002. Morphology and distribution of trichomes in some genera (Morus, Ficus, Broussonetia and Maclura). Iranian Journal of Botany 9: 195-202.
		Morus nigra L.	Leaf	Azizian (2002)Azizian D. 2002. Morphology and distribution of trichomes in some genera (Morus, Ficus, Broussonetia and Maclura). Iranian Journal of Botany 9: 195-202.
		Streblus asper Lour.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
	Urticaceae	Boehmeria caudata Sw.	Leaf	*Fernandez et al. (2011*Fernandez RD, Cabrera CN, Albornoz PL, Arias ME. 2011. Anatomía foliar de Boehmeria caudata (Urticaceae) em la provincia de Tucumán, Argentina. Lilloa 48: 53-59.)
		Fleurya interrupta (L.) Gaudich.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Girardinia diversifolia (Link) Friis	Leaf	*Fu et al. (2003*Fu HY, Chen SJ, Huang LLK. 2003. Comparative study on the stinging trichomes and some related epidermal structure in the leaves of Dendrocnide meyeniana, Girardinia diversifolia, and Urtica thunbergiana. Taiwania 48: 213-223.)
		Pouzolzia zeylanica (L.) Benn. & R.Br.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
Capitate: unicellular stalk and pluricellular head constituted from four cells or more	Moraceae	Artocarpus heterophyllus Lam.	Leaf, inflorescence peduncle	*Schnetzler et al. (2017*Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.)
		Broussonetia papyrifera (L.) L’Hér. ex Vent.	Leaf	Shah & Kachroo (1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.)
		Ficus carica L.	Leaf	Azizian (2002)Azizian D. 2002. Morphology and distribution of trichomes in some genera (Morus, Ficus, Broussonetia and Maclura). Iranian Journal of Botany 9: 195-202.
		Ficus heterophylla L. f.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus hispida L. f.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus racemosa L.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Ficus repens Hook. Ex Miq.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Maclura tinctoria (L.) D. Don ex Steud.	Stem, leaf	*Schnetzler et al. (2017*Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.)
		Morus alba L.	Stem, leaf	Shah & Kachro (1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.)
		Morus alba L.	Leaf	Gangadhara and Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.); Azizian (2002)Azizian D. 2002. Morphology and distribution of trichomes in some genera (Morus, Ficus, Broussonetia and Maclura). Iranian Journal of Botany 9: 195-202.
		Sorocea bonplandii (Baill.) W.C. Burger, Lanj. & Wess. Boer	Stem, leaf, flower	*Schnetzler et al. (2017*Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.)
		Streblus asper Lour.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.); Shah & Kachoroo (1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.)
	Ulmaceae	Ampelocera glabra Kuhlm.	Stem, leaf, bract	*Leme et al.* (2018**Leme FM, Staedler YM, Schonenberger J, Teixeira SP. 2018. Ontogeny and vascularization elucidate the atypical floral structure of Ampelocera glabra, a tropical species of Ulmaceae. International Journal of Plant Science 179: 461-476.); This study
		Phyllostylon rhamnoides (J. Poiss) Taub.	Stem, leaf	This study
		Ulmus parvifolia Jacq.	Stem, leaf, bract	This study
		Zelkova serrata (Thunb.) Makino	Stem, leaf, flower	This study
	Urticaceae	Boehmeria caudata Sw.	Leaf	*Fernandez et al. (2011*Fernandez RD, Cabrera CN, Albornoz PL, Arias ME. 2011. Anatomía foliar de Boehmeria caudata (Urticaceae) em la provincia de Tucumán, Argentina. Lilloa 48: 53-59.)
		Dendrocnide meyeniana (Walp.) Chew	Leaf	*Fu et al. (2003*Fu HY, Chen SJ, Huang LLK. 2003. Comparative study on the stinging trichomes and some related epidermal structure in the leaves of Dendrocnide meyeniana, Girardinia diversifolia, and Urtica thunbergiana. Taiwania 48: 213-223.)
		Urtica dioica L. (Ur)	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Urtica thumbergiana Siebold & Zucc.	Leaf	*Fu et al. (2003*Fu HY, Chen SJ, Huang LLK. 2003. Comparative study on the stinging trichomes and some related epidermal structure in the leaves of Dendrocnide meyeniana, Girardinia diversifolia, and Urtica thunbergiana. Taiwania 48: 213-223.)
Capitate: uniseriate and bicellular stalk, and pluricellular head	Moraceae	Ficus racemosa L.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
Capitate: biseriate stalk with two cells in each series, and head from four to eight cells (bulbous)	Cannabaceae	Cannabis sativa L.	Bract	Hammond & Malhberg (1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.); Dayanandan & Kaufman (1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.); Briosi & Togni (1894)Briosi G, Tognini F. 1894. Anatomia Della Canapa (Cannabis sativa L.). Milano, Istituto Botanico Della R, Universitá Di Pavia.
	Cannabaceae	Humulus lupulus L.	Leaf, bract	*Oliveira et al. (1988*Oliveira MM, Salomk M, Pais M. 1988. Glandular trichomes of Humulus lupulus var. Brewer’s Gold: ontogeny and histochemical characterization of the secretion. Nordic Journal Botany 8: 349-359.)
Capitate: biseriate stalk with two cells in each series and disc-shaped head formed by a layer of cells (peltate)	Cannabaceae	Cannabis sativa L.	Bract, flower (stamen)	Dayanandan & Kaufman (1976Dayanandan P, Kaufman PB. 1976. Trichomes of Cannabis sativa L. (Cannabaceae). American Journal of Botany 63: 578-591.); Hammond & Malhberg (1977Hammond CT, Mahlberg PG. 1977. Morphogenesis of capitate glandular hairs of Cannabis sativa (Cannabaceae). American Journal of Botany 64: 1023-1031.); *Leme et al. (2020*Leme FM, Schönenberger J, Staedler YM, Teixeira SP. 2020. Comparative floral development reveals novel aspects of structure and diversity of flowers in Cannabaceae. Botanical Journal of Linnean Society 193: 64-83.)
		Cannabis sativa L.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Humulus lupulus L.	Leaf, bract	*Oliveira et al. (1988*Oliveira MM, Salomk M, Pais M. 1988. Glandular trichomes of Humulus lupulus var. Brewer’s Gold: ontogeny and histochemical characterization of the secretion. Nordic Journal Botany 8: 349-359.)
Capitate: peltate head (cells radially arranged)	Moraceae	Artocarpus altilis (Parkinson) Fosberg (syn. Artocarpus incisa)	Leaf	Shah & Kachroo (1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.)
		Artocarpus heterophyllus Lam.	Leaf	*Schnetzler et al. (2017*Schnetzler BN, Teixeira SP, Marinho CR. 2017. Trichomes that secrete substances of a mixed nature in the vegetative and reproductive organs of some species of Moraceae. Acta Botanica Brasilica 31: 392-402.)
		Brosimum gaudichaudii Trécul	Bract	*Jacomassi et al. (2010*Jacomassi E, Moscheta IS, Machado SR. 2010. Morfoanatomia e histoquímica de órgãos reprodutivos de Brosimum gaudichaudii (Moraceae). Brazilian Journal of Botany 33: 115-129.)
Capitate: uniseriate and bicellular stalk, and head with three to seven cells (peltate)	Moraceae	Broussonetia papyrifera (L.) L’Hér.ex Vent.	Leaf	Shah & Kachroo (1975Shah AM, Kachroo P. 1975. Comparative anatomy in Urticales I. The trichomes in Moraceace. Journal Indian Botany Society 54: 138-153.)
Capitate: biseriate stalk with several cells in each series and pluricellular head	Cannabaceae	Pteroceltis tatarinowii Maxim.	Leaf	This study
	Cannabaceae	Trema micrantha (L.) Blume	Leaf	This study
Filiform short (short clavate): up to four linear cells	Cannabaceae	Lozanella enantiophylla (Donn. Sm.) Killip & C.V. Morton	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
	Cannabaceae	Lozanella permollis Killip & C. V. Morton	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
	Ulmaceae	Hemiptelea davidii (Hance) Planch.	Leaf, flower (ovary)	Tobe and Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Holoptelea integrifolia Planch.	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Phyllostylon brasiliensis Capan. Ex Benth. & Hook. f.	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Planera aquatica J. F. Gmel.	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Ulmus davidiana Planch.	Flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Ulmus laciniata (Trautv.) Mayr	Flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Ulmus parvifolia Jacq.	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Zelkova schneidriana Hand. Mazz.	Flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Zelkova serrata (Thunb.) Makino	Flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
Filiform long (long clavate): uniseriate, with more of four linear cells	Cannabaceae	Aphananthe aspera (Thunb.) Planch.	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Celtis sp.	Leaf	Gangadhara & Inamdar (1977Gangadhara M, Inamdar JA. 1977. Trichomes and stomata, and their taxonomic significance in the Urticales. Plant Systematic and Evolution 127: 121-137.)
		Celtis pubescens Spreng	Stem, leaf, flower	This study
		Celtis boninensis Koidz	Leaf	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Celtis sinensis Pers.	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Celtis spinosa Spreng.	Leaf	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Lozanella permollis Killip & C. V. Morton	Leaf, flower (ovary)	Tobe and Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Parasponia rigida Merr. & Perry	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Pteroceltis tatarinowii Maxim.	Leaf, flower (ovary)	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Trema lamarkiana (Roem. & Schult.) Blume	Leaf	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Trema micrantha (L.) Blume	Leaf	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
	Ulmaceae	Ampelocera ruzzi Klotzsch	Leaf	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
Filiform: biseriate (long clavate biseriate)	Cannabaceae	Chaetachme aristata E. Mey. Ex Planch.	Leaf	Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)
		Trema micrantha (L.) Blume	Stem, leaf, flower	This study
		Trema politoria (Planch.) Blume	Leaf	Bhat & Kachroo (1979Bhat MM, Kachroo P. 1979. The trichome in phylogeny of Urticales. Annual Reviews of Plant Sciences 1: 375-407.) apud Tobe & Takaso (1996Tobe H, Takaso T. 1996. Trichome micromorphology in Celtidaceae and Ulmaceae (Urticales). Acta Phytotaxonomica et Geobotanica 47: 153-168.)

Trichome type	Species	Stem	Petiole	Leaf blade	Pedicel	Sepal	Stamen	Pistil
capitate with uniseriate stalk (type 3)	Celtis pubescens	+	+	+	+	+	-	-
capitate with biseriate stalk (type 12)	Pteroceltis tatarinowii	+	+	+	+	+	-	+
capitate with biseriate stalk (type 12)	Trema micrantha	+	+	+	+	+	-	-
capitate with unicellular stalk (type 6)	Ampelocera glabra	+	+	+	-	+	-	+
	Phyllostylon rhamnoides	+	+	+
	Ulmus parvifolia	+	+	+
	Zelkova serrata	+	+	+	-	-	-	+
uniseriate filiform (type 14)	Celtis pubescens	+	+	+	+	+	-	+
biseriate filiform (type 15)	Trema micrantha	+	+	+	+	+	-	-

Sociedade Botânica do Brasil SCLN 307 - Bloco B - Sala 218 - Ed. Constrol Center Asa Norte CEP: 70746-520 Brasília/DF. - Alta Floresta - MT - Brazil
E-mail: acta@botanica.org.br

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